Eradication of gastric cancer is now both possible and practical

Seminars in Cancer Biology

Volumn 23, Issue 6 PB, 2013, Pages 492-501

  Shiotani, Akiko ^a   Cen, Putao ^b   Graham, David Y ^c  

^a KAWASAKI MEDICAL SCHOOL   (Japan)

^b UNIVERSITY OF TEXAS   (United States)

^c MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Atrophic gastritis; Cancer screening; Gastric cancer; Helicobacter pylori; Natural history; Pepsinogen; Prevention; Primary prevention; Risk; Secondary prevention; Surveillance

Indexed keywords

BACTERIUM ANTIBODY; PEPSINOGEN I; PEPSINOGEN II;

ACHLORHYDRIA; ATROPHIC GASTRITIS; CANCER INCIDENCE; CANCER PREVENTION; CANCER RISK; DISEASE ERADICATION; DRUG SURVEILLANCE PROGRAM; ERADICATION THERAPY; GASTRITIS; GENETIC RISK; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; IMMUNOASSAY; NONHUMAN; PRIMARY PREVENTION; PROTEIN BLOOD LEVEL; REVIEW; RISK ASSESSMENT; RISK MANAGEMENT; RISK REDUCTION; SECONDARY PREVENTION; SEROLOGY; STOMACH CANCER; STOMACH MUCOSA;

ACTIVATION-INDUCED CYTIDINE DEAMINASE; AID; ATROPHIC GASTRITIS; BRCA1; BREAST CANCER SUSCEPTIBILITY GENE 1; CADHERIN-1; CANCER SCREENING; CDH1; CDKN2A; CI; CONFIDENCE INTERVAL; CPG; CYCLIN-DEPENDENT KINASE INHIBITOR 2A; CYTOSINE-PHOSPHATE-GUANINE ARE REGIONS OF DNA; GASTRIC CANCER; GASTROINTESTINAL; GI; H. PYLORI; HELICOBACTER PYLORI; HMLH1; HUMAN MUTL HOMOLOG 1; IARC; INTERNATIONAL AGENCY FOR RESEARCH ON CANCER; KLF5; KRÜPPEL-LIKE FACTOR 5; METHYLATED-DNA-PROTEIN-CYSTEINE METHYLTRANSFERASE; MGMT; MLH1; MUTL HOMOLOG 1; NATURAL HISTORY; OLGA; OPERATIVE LINK ON GASTRITIS ASSESSMENT; PEPSINOGEN; PREVENTION; PRIMARY PREVENTION; RISK; RUNT-RELATED TRANSCRIPTION FACTOR 3; RUNX3; SECONDARY PREVENTION; SURVEILLANCE; VALOSIN-CONTAINING PROTEIN; VCP;

GASTRITIS; HELICOBACTER INFECTIONS; HISTORY, 20TH CENTURY; HUMANS; INCIDENCE; RESEARCH; RISK; STOMACH NEOPLASMS;

EID: 84887618651     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2013.07.004     Document Type: Review

References (87)

1. Melton S.D., Genta R.M., Souza R.F. Biomarkers and molecular diagnosis of gastrointestinal and pancreatic neoplasms. Nature Reviews Gastroenterology & Hepatology 2010, 7:620-628.
2. Correa P., Houghton J. Carcinogenesis of Helicobacter pylori. Gastroenterology 2007, 133:659-672.
3. Hoffman F.L. The mortality from cancer throughout the world 1915, Prudential Press, Newark.
4. IARC Helicobacter pylori. Biologic agents: a review of human carcinogens 2012, 385-435. International Agency for Research on Cancer, Leon.
5. Sipponen P., Helske T., Jarvinen P., Hyvarinen H., Seppala K., Siurala M. Fall in the prevalence of chronic gastritis over 15 years: analysis of outpatient series in Finland from 1977, 1985, and 1992. Gut 1994, 35:1167-1171.
6. Sipponen P., Kimura K. Intestinal metaplasia, atrophic gastritis and stomach cancer: trends over time. European Journal of Gastroenterology and Hepatology 1994, 6(Suppl. 1):79-83.
7. Graham D.Y., Lu H., African Yamaoka Y. Asian or Indian enigma, the East Asian Helicobacter pylori: facts or medical myths. Journal of Digestive Diseases 2009, 10:77-84.
8. IARC IARC monographs on the evaluation of carcinogenic risks to humans (vol. 61): schistosomes, liver flukes and Helicobacter pylori 1994, International Agency for Research on Cancer, Lyon, France.
9. Graham D.Y., Asaka M. Eradication of gastric cancer and more efficient gastric cancer surveillance in Japan: two peas in a pod. Journal of Gastroenterology 2010, 45:1-8.
10. Kokkola A., Kosunen T.U., Puolakkainen P., Sipponen P., Harkonen M., Laxen F., et al. Spontaneous disappearance of Helicobacter pylori antibodies in patients with advanced atrophic corpus gastritis. APMIS 2003, 111:619-624.
11. Ekstrom A.M., Held M., Hansson L.E., Engstrand L., Nyren O. Helicobacter pylori in gastric cancer established by CagA immunoblot as a marker of past infection. Gastroenterology 2001, 121:784-791.
12. Weck M.N., Gao L., Brenner H. Helicobacter pylori infection and chronic atrophic gastritis: associations according to severity of disease. Epidemiology 2009, 20:569-574.
13. Comfort M.W. Gastric acidity before and after development of gastric cancer: its etiologic, diagnostic and prognostic significance. Annals of Internal Medicine 1951, 36:1331-1348.
14. Faber K. Gastritis and its consequences 1935, Oxford University Press, Paris.
15. Lauren P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathologica et Microbiologica Scandinavica 1965, 64:31-49.
16. Jarvi O., Lauren P. On the role of heterotopias of the intestinal epithelium in the pathogenesis of gastric cancer. Acta Pathologica et Microbiologica Scandinavica 1951, 29:26-44.
17. Correa P., Haenszel W., Cuello C., Tannenbaum S., Archer M. A model for gastric cancer epidemiology. Lancet 1975, 2:58-60.
18. Correa P., Cuello C., Duque E., Burbano L.C., Garcia F.T., Bolanos O., et al. Gastric cancer in Colombia. III. Natural history of precursor lesions. Journal of the National Cancer Institute 1976, 57:1027-1035.
19. Correa P., Cuello C., Duque E. Carcinoma and intestinal metaplasia of the stomach in Colombian migrants. Journal of the National Cancer Institute 1970, 44:297-306.
20. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process - First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Research 1992, 52:6735-6740.
21. Pritchard D.M., Crabtree J.E. Helicobacter pylori and gastric cancer. Current Opinion in Gastroenterology 2006, 22:620-625.
22. Takaishi S., Okumura T., Wang T.C. Gastric cancer stem cells. Journal of Clinical Oncology 2008, 26:2876-2882.
23. Kakinoki R., Kushima R., Matsubara A., Saito Y., Okabe H., Fujiyama Y., et al. Re-evaluation of histogenesis of gastric carcinomas: a comparative histopathological study between Helicobacter pylori-negative and H. pylori-positive cases. Digestive Diseases and Sciences 2009, 54:614-620.
24. Mesquita P., Raquel A., Nuno L., Reis C.A., Silva L.F., Serpa J., et al. Metaplasia - a transdifferentiation process that facilitates cancer development: the model of gastric intestinal metaplasia. Critical Reviews in Oncogenesis 2006, 12:3-26.
25. Meining A., Morgner A., Miehlke S., Bayerdorffer E., Stolte M. Atrophy-metaplasia-dysplasia-carcinoma sequence in the stomach: a reality or merely an hypothesis. Best Practice and Research Clinical Gastroenterology 2001, 15:983-998.
26. Shiotani A., Haruma K., Uedo N., Iishi H., Ishihara R., Tatsuta M., et al. Histological risk markers for non-cardia early gastric cancer: pattern of mucin expression and gastric cancer. Virchows Archiv 2006.
27. Shiotani A., Iishi H., Uedo N., Ishiguro S., Tatsuta M., Nakae Y., et al. Evidence that loss of sonic hedgehog is an indicator of Helicobacter pylori-induced atrophic gastritis progressing to gastric cancer. American Journal of Gastroenterology 2005, 100:581-587.
28. Shiotani A., Iishi H., Uedo N., Kumamoto M., Nakae Y., Ishiguro S., et al. Histologic and serum risk markers for noncardia early gastric cancer. International Journal of Cancer 2005, 115:463-469.
29. Cheli R., Perasso A., Giacosa A. Gastritis a clinical review 1987, Springer-Verlag, Berlin.
30. Kimura K. Chronological transition of the fundic-pyloric border determined by stepwise biopsy of the lesser and greater curvatures of the stomach. Gastroenterology 1972, 63:584-592.
31. Satoh K., Kimura K., Taniguchi Y., Yoshida Y., Kihira K., Takimoto T., et al. Distribution of inflammation and atrophy in the stomach of Helicobacter pylori-positive and -negative patients with chronic gastritis. American Journal of Gastroenterology 1996, 91:963-969.
32. El-Zimaity H.M., Ota H., Graham D.Y., Akamatsu T., Katsuyama T. Patterns of gastric atrophy in intestinal type gastric carcinoma. Cancer 2002, 94:1428-1436.
33. Sipponen P., Graham D.Y. Importance of atrophic gastritis in diagnostics and prevention of gastric cancer: application of plasma biomarkers. Scandinavian Journal of Gastroenterology 2007, 42:2-10.
34. Kokkola A., Sipponen P., Rautelin H., Harkonen M., Kosunen T.U., Haapiainen R., et al. The effect of Helicobacter pylori eradication on the natural course of atrophic gastritis with dysplasia. Alimentary Pharmacology and Therapeutics 2002, 16:515-520.
35. Gutierrez O., Melo M., Segura A.M., Angel A., Genta R.M., Graham D.Y. Cure of Helicobacter pylori infection improves gastric acid secretion in patients with corpus gastritis. Scandinavian Journal of Gastroenterology 1997, 32:664-668.
36. Graham D.Y., Shiotani A., El-Zimaity H.M. Chromoendoscopy points the way to understanding recovery of gastric function after Helicobacter pylori eradication. Gastrointestinal Endoscopy 2006, 64:686-690.
37. Shiotani A., Murao T., Uedo N., Iishi H., Yamanaka Y., Kamada T., et al. Eradication of H. pylori did not improve abnormal sonic hedgehog expression in the high risk group for gastric cancer. Digestive Diseases and Sciences 2012, 57:643-649.
38. Shiotani A., Uedo N., Iishi H., Murao T., Kanzaki T., Kimura Y., et al. H. pylori eradication did not improve dysregulation of specific oncogenic miRNAs in intestinal metaplastic glands. Journal of Gastroenterology 2012, 47:988-998.
39. Fukase K., Kato M., Kikuchi S., Inoue K., Uemura N., Okamoto S., et al. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet 2008, 372:392-397.
40. Wu C.Y., Kuo K.N., Wu M.S., Chen Y.J., Wang C.B., Lin J.T. Early Helicobacter pylori eradication decreases risk of gastric cancer in patients with peptic ulcer disease. Gastroenterology 2009, 137:1641-1648.
41. Lee Y.C., Chen T.H., Chiu H.M., Shun C.T., Chiang H., Liu T.Y., et al. The benefit of mass eradication of Helicobacter pylori infection: a community-based study of gastric cancer prevention. Gut 2012.
42. Graham D.Y., Uemura N. Natural history of gastric cancer after Helicobacter pylori eradication in Japan: after endoscopic resection, after treatment of the general population, and naturally. Helicobacter 2006, 11:139-143.
43. Ma J.L., Zhang L., Brown L.M., Li J.Y., Shen L., Pan K.F., et al. Fifteen-year effects of Helicobacter pylori, garlic, and vitamin treatments on gastric cancer incidence and mortality. Journal of the National Cancer Institute 2012, 104:488-492.
44. Chiba T., Marusawa H., Ushijima T. Inflammation-associated cancer development in digestive organs: mechanisms and roles for genetic and epigenetic modulation. Gastroenterology 2012, 143:550-563.
45. Ushijima T., Hattori N. Molecular pathways: involvement of Helicobacter pylori-triggered inflammation in the formation of an epigenetic field defect, and its usefulness as cancer risk and exposure markers. Clinical Cancer Research 2012, 18:923-929.
46. Sjoblom T., Jones S., Wood L.D., Parsons D.W., Lin J., Barber T.D., et al. The consensus coding sequences of human breast and colorectal cancers. Science 2006, 314:268-274.
47. Pleasance E.D., Stephens P.J., O'Meara S., McBride D.J., Meynert A., Jones D., et al. A small-cell lung cancer genome with complex signatures of tobacco exposure. Nature 2010, 463:184-190.
48. Stephens P.J., McBride D.J., Lin M.L., Varela I., Pleasance E.D., Simpson J.T., et al. Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 2009, 462:1005-1010.
49. Niwa T., Tsukamoto T., Toyoda T., Mori A., Tanaka H., Maekita T., et al. Inflammatory processes triggered by Helicobacter pylori infection cause aberrant DNA methylation in gastric epithelial cells. Cancer Research 2010, 70:1430-1440.
50. Maekita T., Nakazawa K., Mihara M., Nakajima T., Yanaoka K., Iguchi M., et al. High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk. Clinical Cancer Research 2006, 12:989-995.
51. Hattori T. Development of adenocarcinomas in the stomach. Cancer 1986, 57:1528-1534.
52. Kodama M., Tur G.E., Shiozawa N., Koyama K. Clinicopathological features of multiple primary gastric carcinoma. Journal of Surgical Oncology 1996, 62:57-61.
53. Shimizu T., Marusawa H., Endo Y., Chiba T. Inflammation-mediated genomic instability: roles of activation-induced cytidine deaminase in carcinogenesis. Cancer Science 2012, 103:1201-1206.
54. Iijima K., Sekine H., Koike T., Imatani A., Ohara S., Shimosegawa T. Long-term effect of Helicobacter pylori eradication on the reversibility of acid secretion in profound hypochlorhydria. Alimentary Pharmacology and Therapeutics 2004, 19:1181-1188.
55. Houben G.M., Stockbrugger R.W. Bacteria in the aetio-pathogenesis of gastric cancer: a review. Scandinavian Journal of Gastroenterology. Supplement 1995, 212:13-18.
56. Forsythe S.J., Dolby J.M., Webster A.D., Cole J.A. Nitrate- and nitrite-reducing bacteria in the achlorhydric stomach. Journal of Medical Microbiology 1988, 25:253-259.
57. Toller I.M., Neelsen K.J., Steger M., Hartung M.L., Hottiger M.O., Stucki M., et al. Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:14944-14949.
58. Kim J.J., Tao H., Carloni E., Leung W.K., Graham D.Y., Sepulveda A.R. Helicobacter pylori impairs DNA mismatch repair in gastric epithelial cells. Gastroenterology 2002, 123:542-553.
59. Conticello S.G. The AID/APOBEC family of nucleic acid mutators. Genome Biology 2008, 9:229.
60. Matsumoto Y., Marusawa H., Kinoshita K., Endo Y., Kou T., Morisawa T., et al. Helicobacter pylori infection triggers aberrant expression of activation-induced cytidine deaminase in gastric epithelium. Nature Medicine 2007, 13:470-476.
61. Shin C.M., Kim N., Jung Y., Park J.H., Kang G.H., Park W.Y., et al. Genome-wide DNA methylation profiles in noncancerous gastric mucosae with regard to Helicobacter pylori infection and the presence of gastric cancer. Helicobacter 2011, 16:179-188.
62. Zabaleta J. MicroRNA: a bridge from H. pylori infection to gastritis and gastric cancer development. Frontiers in Genetics 2012, 3:294.
63. Noto J.M., Khizanishvili T., Chaturvedi R., Piazuelo M.B., Romero-Gallo J., Delgado A.G., et al. Helicobacter pylori promotes the expression of kruppel-like factor 5, a mediator of carcinogenesis, in vitro and in vivo. PLoS ONE 2013, 8:e54344.
64. Yu C.C., Yang J.C., Chang Y.C., Chuang J.G., Lin C.W., Wu M.S., et al. VCP phosphorylation-dependent interaction partners prevent apoptosis in Helicobacter pylori-infected gastric epithelial cells. PLoS ONE 2013, 8:e55724.
65. Graham D.Y., Shiotani A. The time to eradicate gastric cancer is now. Gut 2005, 54:735-738.
66. Shiotani A., Uedo N., Iishi H., Yoshiyuki Y., Ishii M., Manabe N., et al. Predictive factors for metachronous gastric cancer in high-risk patients after successful Helicobacter pylori eradication. Digestion 2008, 78:113-119.
67. Asaka M. A new approach for elimination of gastric cancer deaths in Japan. International Journal of Cancer 2013, 132:1272-1276.
68. Trends in age-specific incidence rate. Cancer statistics in Japan - 2011 2011, 29-36. Foundation for Promotion of Cancer Research, Tokyo.
69. Sipponen P., Kekki M., Haapakoski J., Ihamäki T., Siurala M. Gastric cancer risk in chronic atrophic gastritis: statistical calculations of cross-sectional data. International Journal of Cancer 1985, 35:173-177.
70. Fry J. Peptic ulcer: a profile. British Medical Journal 1964, 2:809-812.
71. Ubukata H., Nagata H., Tabuchi T., Konishi S., Kasuga T., Tabuchi T. Why is the coexistence of gastric cancer and duodenal ulcer rare? Examination of factors related to both gastric cancer and duodenal ulcer. Gastric Cancer 2011, 14:4-12.
72. Nomura A.M., Stemmermann G.N., Samloff I.M. Serum pepsinogen I as a predictor of stomach cancer. Annals of Internal Medicine 1980, 93:537-540.
73. Miki K. Gastric cancer screening using the serum pepsinogen test method. Gastric Cancer 2006, 9:245-253.
74. Iijima K., Abe Y., Kikuchi R., Koike T., Ohara S., Sipponen P., et al. Serum biomarker tests are useful in delineating between patients with gastric atrophy and normal, healthy stomach. World Journal of Gastroenterology 2009, 15:853-859.
75. Vaananen H., Vauhkonen M., Helske T., Kaariainen I., Rasmussen M., Tunturi-Hihnala H., et al. Non-endoscopic diagnosis of atrophic gastritis with a blood test. Correlation between gastric histology and serum levels of gastrin-17 and pepsinogen I: a multicentre study. European Journal of Gastroenterology and Hepatology 2003, 15:885-891.
76. Brenner H., Rothenbacher D., Weck M.N. Epidemiologic findings on serologically defined chronic atrophic gastritis strongly depend on the choice of the cutoff-value. International Journal of Cancer 2007, 121:2782-2786.
77. Ohata H., Kitauchi S., Yoshimura N., Mugitani K., Iwane M., Nakamura H., et al. Progression of chronic atrophic gastritis associated with Helicobacter pylori infection increases risk of gastric cancer. International Journal of Cancer 2004, 109:138-143.
78. Watabe H., Mitsushima T., Yamaji Y., Okamoto M., Wada R., Kokubo T., et al. Predicting the development of gastric cancer from combining Helicobacter pylori antibodies and serum pepsinogen status: a prospective endoscopic cohort study. Gut 2005, 54:764-768.
79. Kudo T., Kakizaki S., Sohara N., Onozato Y., Okamura S., Inui Y., et al. Analysis of ABC (D) stratification for screening patients with gastric cancer. World Journal of Gastroenterology 2011, 17:4793-4798.
80. Shimoyama T., Aoki M., Sasaki Y., Matsuzaka M., Nakaji S., Fukuda S. ABC screening for gastric cancer is not applicable in a Japanese population with high prevalence of atrophic gastritis. Gastric Cancer 2012, 15:331-334.
81. Miki K. Gastric cancer screening by combined assay for serum anti-Helicobacter pylori IgG antibody and serum pepsinogen levels - ABC method. Proceedings of the Japan Academy - Series B: Physical & Biological Sciences 2011, 87:405-414.
82. Kaise M., Miwa J., Fujimoto A., Tashiro J., Tagami D., Sano H., et al. Influence of Helicobacter pylori status and eradication on the serum levels of trefoil factors and pepsinogen test: serum trefoil factor 3 is a stable biomarker. Gastric Cancer 2012.
83. Kawai T., Miki K., Ichinose M., Kenji Y., Miyazaki I., Kawakami K., et al. Changes in evaluation of the pepsinogen test result following Helicobacter pylori eradication therapy in Japan. Inflammopharmacology 2007, 15:31-35.
84. Capelle L.G., de Vries A.C., Haringsma J., Ter B.F., de Vries R.A., Bruno M.J., et al. The staging of gastritis with the OLGA system by using intestinal metaplasia as an accurate alternative for atrophic gastritis. Gastrointestinal Endoscopy 2010, 71:1150-1158.
85. Rugge M., Correa P., Di M.F., el-Omar E., Fiocca R., Geboes K., et al. OLGA staging for gastritis: a tutorial. Digestive and Liver Disease 2008, 40:650-658.
86. Wong B.C., Zhang L., Ma J.L., Pan K.F., Li J.Y., Shen L., et al. Effects of selective COX-2 inhibitor and Helicobacter pylori eradication on precancerous gastric lesions. Gut 2012, 61:812-818.
87. Nardone G., Rocco A. Chemoprevention of gastric cancer: role of COX-2 inhibitors and other agents. Digestive Diseases 2004, 22:320-326.