Helicobacter pylori associated chronic gastritis, clinical syndromes, precancerous lesions, and pathogenesis of gastric cancer development

World Journal of Gastroenterology

Volumn 20, Issue 18, 2014, Pages 5461-5473

  Watari, Jiro ^a   Chen, Nancy ^b   Amenta, Peter S ^b   Fukui, Hirokazu ^a   Oshima, Tadayuki ^a   Tomita, Toshihiko ^a   Miwa, Hiroto ^a   Lim, Kheng Jim ^b   Das, Kiron M ^b  

^a HYOGO COLLEGE OF MEDICINE   (Japan)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Eradication; Gastric atrophy; Gastric cancer; Helicobacter pylori; Intestinal metaplasia; Molecular alteration; Prevention

Indexed keywords

CAGA PROTEIN; MOLECULAR MARKER; PEPSINOGEN I; PEPSINOGEN II; VACUOLATING TOXIN; ANTIINFECTIVE AGENT;

ATROPHIC GASTRITIS; BACTERIAL CLEARANCE; BACTERIAL GENE; CANCER STAGING; CARCINOGENESIS; CHRONIC GASTRITIS; CLINICAL TRIAL (TOPIC); DYSPEPSIA; ENDOSCOPIC SURGERY; EPIGENETICS; GASTROESOPHAGEAL REFLUX; GENETIC VARIABILITY; GEOGRAPHIC PATHOLOGY; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HETEROZYGOSITY LOSS; HIGH RISK PATIENT; HUMAN; INTESTINE METAPLASIA; META ANALYSIS (TOPIC); METHYLATION; MICROSATELLITE INSTABILITY; MULTICENTER STUDY (TOPIC); NONHUMAN; PEPTIC ULCER; PRECANCER; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SENSITIVITY AND SPECIFICITY; STOMACH CANCER; SYSTEMATIC REVIEW (TOPIC); TUMOR SUPPRESSOR GENE; ANIMAL; CHRONIC DISEASE; DRUG EFFECTS; GASTRITIS; GENETICS; HELICOBACTER INFECTIONS; MICROBIOLOGY; PATHOGENICITY; PRECANCEROUS CONDITIONS; RISK FACTOR; STOMACH NEOPLASMS; TREATMENT OUTCOME;

ANIMALS; ANTI-BACTERIAL AGENTS; CHRONIC DISEASE; GASTRITIS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; PRECANCEROUS CONDITIONS; RISK FACTORS; STOMACH NEOPLASMS; TREATMENT OUTCOME;

EID: 84900428907     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i18.5461     Document Type: Review

References (149)

1. Cave DR. Transmission and epidemiology of Helicobacter pylori. Am J Med 1996; 100: 12S-17S; discussion 17S-18S [PMID: 8644777]
2. Siao D, Somsouk M. Helicobacter pylori: evidence-based review with a focus on immigrant populations. J Gen Intern Med 2014; 29: 520-528 [PMID: 24065381 DOI: 10.1007/ s11606-013-2630-y]
3. Hosseini E, Poursina F, de Wiele TV, Safaei HG, Adibi P. Helicobacter pylori in Iran: A systematic review on the association of genotypes and gastroduodenal diseases. J Res Med Sci 2012; 17: 280-292 [PMID: 23267382]
4. Schwarz S, Morelli G, Kusecek B, Manica A, Balloux F, Owen RJ, Graham DY, van der Merwe S, Achtman M, Suerbaum S. Horizontal versus familial transmission of Helicobacter pylori. PLoS Pathog 2008; 4: e1000180 [PMID: 18949030 DOI: 10.1371/journal.ppat.1000180]
5. Magalhães Queiroz DM, Luzza F. Epidemiology of Helicobacter pylori infection. Helicobacter 2006; 11 Suppl 1: 1-5 [PMID: 16925604 DOI: 10.1111/j.1478-405X.2006.00429.x]
6. Thomas JE, Gibson GR, Darboe MK, Dale A, Weaver LT. Isolation of Helicobacter pylori from human faeces. Lancet 1992; 340: 1194-1195 [PMID: 1359263]
7. Axon AT. Review article: is Helicobacter pylori transmitted by the gastro-oral route? Aliment Pharmacol Ther 1995; 9: 585-588 [PMID: 8824644]
8. Calvet X, Ramírez Lázaro MJ, Lehours P, Mégraud F. Diagnosis and epidemiology of Helicobacter pylori infection. Helicobacter 2013; 18 Suppl 1: 5-11 [PMID: 24011238 DOI: 10.1111/hel.12071]
9. Pounder RE, Ng D. The prevalence of Helicobacter pylori infection in different countries. Aliment Pharmacol Ther 1995; 9 Suppl 2: 33-39 [PMID: 8547526]
10. Hu LT, Foxall PA, Russell R, Mobley HL. Purification of recombinant Helicobacter pylori urease apoenzyme encoded by ureA and ureB. Infect Immun 1992; 60: 2657-2666 [PMID: 1612735]
11. Logan RP. Adherence of Helicobacter pylori. Aliment Pharmacol Ther 1996; 10 Suppl 1: 3-15 [PMID: 8730255]
12. Liu H, Semino-Mora C, Dubois A. Mechanism of H. pylori intracellular entry: an in vitro study. Front Cell Infect Microbiol 2012; 2: 13 [PMID: 22919605 DOI: 10.3389/fcimb.2012.00013]
13. Chey WD, Wong BC. American College of Gastroenterology guideline on the management of Helicobacter pylori infection. Am J Gastroenterol 2007; 102: 1808-1825 [PMID: 17608775 DOI: 10.1111/j.1572-0241.2007.01393.x]
14. DuBois S, Kearney DJ. Iron-deficiency anemia and Helicobacter pylori infection: a review of the evidence. Am J Gastroenterol 2005; 100: 453-459 [PMID: 15667507 DOI: 10.1111/ j.1572-0241.2005.30252.x]
15. Asahi A, Nishimoto T, Okazaki Y, Suzuki H, Masaoka T, Kawakami Y, Ikeda Y, Kuwana M. Helicobacter pylori eradication shifts monocyte Fcgamma receptor balance toward inhibitory FcgammaRIIB in immune thrombocytopenic purpura patients. J Clin Invest 2008; 118: 2939-2949 [PMID: 18654664 DOI: 10.1172/jci34496]
16. Rostami N, Keshtkar-Jahromi M, Rahnavardi M, Keshtkar-Jahromi M, Esfahani FS. Effect of eradication of Helicobacter pylori on platelet recovery in patients with chronic idiopathic thrombocytopenic purpura: a controlled trial. Am J Hematol 2008; 83: 376-381 [PMID: 18183613 DOI: 10.1002/ ajh.21125]
17. Malfertheiner P, Sipponen P, Naumann M, Moayyedi P, Mégraud F, Xiao SD, Sugano K, Nyrén O. Helicobacter pylori eradication has the potential to prevent gastric cancer: a stateof-the-art critique. Am J Gastroenterol 2005; 100: 2100-2115 [PMID: 16128957 DOI: 10.1111/j.1572-0241.2005.41688.x]
18. Voiosu TA, Giurcan R, Voiosu AM, Voiosu MR. Functional dyspepsia today. Maedica (Buchar) 2013; 8: 68-74 [PMID: 24023602]
19. Zhao B, Zhao J, Cheng WF, Shi WJ, Liu W, Pan XL, Zhang GX. Efficacy of Helicobacter pylori eradication therapy on functional dyspepsia: a meta-analysis of randomized controlled studies with 12-month follow-up. J Clin Gastroenterol 2014; 48: 241-247 [PMID: 24002127 DOI: 10.1097/ MCG.0b013e31829f2e25]
20. Suzuki H, Moayyedi P. Helicobacter pylori infection in functional dyspepsia. Nat Rev Gastroenterol Hepatol 2013; 10: 168-174 [PMID: 23358394 DOI: 10.1038/nrgastro.2013.9]
21. Fallone CA, Barkun AN, Friedman G, Mayrand S, Loo V, Beech R, Best L, Joseph L. Is Helicobacter pylori eradication associated with gastroesophageal reflux disease? Am J Gastroenterol 2000; 95: 914-920 [PMID: 10763937 DOI: 10.1111/ j.1572-0241.2000.01929.x]
22. den Hollander WJ, Sostres C, Kuipers EJ, Lanas A. Helicobacter pylori and nonmalignant diseases. Helicobacter 2013; 18. Suppl 1: 24-27 [PMID: 24011241 DOI: 10.1111/hel.12074]
23. Graham DY, Alpert LC, Smith JL, Yoshimura HH. Iatrogenic Campylobacter pylori infection is a cause of epidemic achlorhydria. Am J Gastroenterol 1988; 83: 974-980 [PMID: 3414650]
24. Marshall BJ, Armstrong JA, McGechie DB, Glancy RJ. Attempt to fulfil Koch's postulates for pyloric Campylobacter. Med J Aust 1985; 142: 436-439 [PMID: 3982345]
25. Morris A, Nicholson G. Ingestion of Campylobacter pyloridis causes gastritis and raised fasting gastric pH. Am J Gastroenterol 1987; 82: 192-199 [PMID: 3826027]
26. Fox JG, Correa P, Taylor NS, Zavala D, Fontham E, Janney F, Rodriguez E, Hunter F, Diavolitsis S. Campylobacter pyloriassociated gastritis and immune response in a population at increased risk of gastric carcinoma. Am J Gastroenterol 1989; 84: 775-781 [PMID: 2741887]
27. Rosh JR, Kurfist LA, Benkov KJ, Toor AH, Bottone EJ, Le-Leiko NS. Helicobacter pylori and gastric lymphonodular hyperplasia in children. Am J Gastroenterol 1992; 87: 135-139 [PMID: 1728111]
28. Genta RM, Hamner HW. The significance of lymphoid follicles in the interpretation of gastric biopsy specimens. Arch Pathol Lab Med 1994; 118: 740-743 [PMID: 7517659]
29. Sipponen P, Ranta P, Helske T, Kääriäinen I, Mäki T, Linnala A, Suovaniemi O, Alanko A, Härkönen M. Serum levels of amidated gastrin-17 and pepsinogen I in atrophic gastritis: an observational case-control study. Scand J Gastroenterol 2002; 37: 785-791 [PMID: 12190091]
30. Väänänen H, Vauhkonen M, Helske T, Kääriäinen I, Rasmussen M, Tunturi-Hihnala H, Koskenpato J, Sotka M, Turunen M, Sandström R, Ristikankare M, Jussila A, Sipponen P. 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. Eur J Gastroenterol Hepatol 2003; 15: 885-891 [PMID: 12867799 DOI: 10.1097/01.meg.0000059169.46867.01]
31. Li Z, Zou D, Ma X, Chen J, Shi X, Gong Y, Man X, Gao L, Zhao Y, Wang R, Yan X, Dent J, Sung JJ, Wernersson B, Johansson S, Liu W, He J. Epidemiology of peptic ulcer disease: endoscopic results of the systematic investigation of gastrointestinal disease in China. Am J Gastroenterol 2010; 105: 2570-2577 [PMID: 20736940 DOI: 10.1038/ajg.2010.324]
32. Ciociola AA, McSorley DJ, Turner K, Sykes D, Palmer JB. Helicobacter pylori infection rates in duodenal ulcer patients in the United States may be lower than previously estimated. Am J Gastroenterol 1999; 94: 1834-1840 [PMID: 10406244 DOI: 10.1111/j.1572-0241.1999.01214.x]
33. Jyotheeswaran S, Shah AN, Jin HO, Potter GD, Ona FV, Chey WY. Prevalence of Helicobacter pylori in peptic ulcer patients in greater Rochester, NY: is empirical triple therapy justified? Am J Gastroenterol 1998; 93: 574-578 [PMID: 9576450 DOI: 10.1111/j.1572-0241.1998.167_b.x]
34. Chiorean MV, Locke GR, Zinsmeister AR, Schleck CD, Melton LJ. Changing rates of Helicobacter pylori testing and treatment in patients with peptic ulcer disease. Am J Gastroenterol 2002; 97: 3015-3022 [PMID: 12492184 DOI: 10.1111/ j.1572-0241.2002.07119.x]
35. Nguyen TL, Uchida T, Tsukamoto Y, Trinh DT, Ta L, Mai BH, Le SH, Thai KD, Ho DD, Hoang HH, Matsuhisa T, Okimoto T, Kodama M, Murakami K, Fujioka T, Yamaoka Y, Moriyama M. Helicobacter pylori infection and gastroduodenal diseases in Vietnam: a cross-sectional, hospital-based study. BMC Gastroenterol 2010; 10: 114 [PMID: 20920280 DOI: 10.1186/1471-230x-10-114]
36. Hussein NR. The association of dupA and Helicobacter pylori-related gastroduodenal diseases. Eur J Clin Microbiol Infect Dis 2010; 29: 817-821 [PMID: 20419465 DOI: 10.1007/ s10096-010-0933-z]
37. Zhang Z, Zheng Q, Chen X, Xiao S, Liu W, Lu H. The Helicobacter pylori duodenal ulcer promoting gene, dupA in China. BMC Gastroenterol 2008; 8: 49 [PMID: 18950522 DOI: 10.1186/1471-230x-8-49]
38. Ford AC, Delaney BC, Forman D, Moayyedi P. Eradication therapy for peptic ulcer disease in Helicobacter pylori positive patients. Cochrane Database Syst Rev 2006; (2): CD003840 [PMID: 16625592 DOI: 10.1002/14651858.CD003840.pub4]
39. Ford AC, Delaney BC, Forman D, Moayyedi P. Eradication therapy in Helicobacter pylori positive peptic ulcer disease: systematic review and economic analysis. Am J Gastroenterol 2004; 99: 1833-1855 [PMID: 15330927 DOI: 10.1111/ j.1572-0241.2004.40014.x]
40. Taniyama K, Shimbo T, Iwase H, Tanaka S, Watanabe N, Uemura N. Evidence-based therapy according to the guideline for gastric ulcers is cost-effective in Japan. J Physiol Pharmacol 2011; 62: 627-635 [PMID: 22314565]
41. Hsiao FY, Tsai YW, Wen YW, Kuo KN, Tsai CR, Huang WF. Effect of Helicobacter pylori eradication therapy on risk of hospitalization for a major ulcer event. Pharmacotherapy 2011; 31: 239-247 [PMID: 21361733 DOI: 10.1592/phco.31.3.239]
42. Gisbert JP, Calvet X, Cosme A, Almela P, Feu F, Bory F, Santolaria S, Aznárez R, Castro M, Fernández N, García-Grávalos R, Benages A, Cañete N, Montoro M, Borda F, Pérez-Aisa A, Piqué JM. Long-term follow-up of 1,000 patients cured of Helicobacter pylori infection following an episode of peptic ulcer bleeding. Am J Gastroenterol 2012; 107: 1197-1204 [PMID: 22613904 DOI: 10.1038/ajg.2012.132]
43. Wong CS, Chia CF, Lee HC, Wei PL, Ma HP, Tsai SH, Wu CH, Tam KW. Eradication of Helicobacter pylori for prevention of ulcer recurrence after simple closure of perforated peptic ulcer: a meta-analysis of randomized controlled trials. J Surg Res 2013; 182: 219-226 [PMID: 23158404 DOI: 10.1016/ j.jss.2012.10.046]
44. Correa P. Helicobacter pylori and gastric carcinogenesis. Am J Surg Pathol 1995; 19 Suppl 1: S37-S43 [PMID: 7762738]
45. Huang JQ, Sridhar S, Chen Y, Hunt RH. Meta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer. Gastroenterology 1998; 114: 1169-1179 [PMID: 9609753]
46. Danesh J. Helicobacter pylori infection and gastric cancer: systematic review of the epidemiological studies. Aliment Pharmacol Ther 1999; 13: 851-856 [PMID: 10383517]
47. Fuccio L, Zagari RM, Eusebi LH, Laterza L, Cennamo V, Ceroni L, Grilli D, Bazzoli F. Meta-analysis: can Helicobacter pylori eradication treatment reduce the risk for gastric cancer? Ann Intern Med 2009; 151: 121-128 [PMID: 19620164]
48. Take S, Mizuno M, Ishiki K, Yoshida T, Ohara N, Yokota K, Oguma K, Okada H, Yamamoto K. The long-term risk of gastric cancer after the successful eradication of Helicobacter pylori. J Gastroenterol 2011; 46: 318-324 [PMID: 21103997 DOI: 10.1007/s00535-010-0347-9]
49. Fukase K, Kato M, Kikuchi S, Inoue K, Uemura N, Okamoto S, Terao S, Amagai K, Hayashi S, Asaka M. Effect of eradication of Helicobacter pylori on incidence of metachro-nous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet 2008; 372: 392-397 [PMID: 18675689 DOI: 10.1016/ s0140-6736(08)61159-9]
50. Maehata Y, Nakamura S, Fujisawa K, Esaki M, Moriyama T, Asano K, Fuyuno Y, Yamaguchi K, Egashira I, Kim H, Kanda M, Hirahashi M, Matsumoto T. Long-term effect of Helicobacter pylori eradication on the development of metachronous gastric cancer after endoscopic resection of early gastric cancer. Gastrointest Endosc 2012; 75: 39-46 [PMID: 22018552 DOI: 10.1016/j.gie.2011.08.030]
51. Kato M, Nishida T, Yamamoto K, Hayashi S, Kitamura S, Yabuta T, Yoshio T, Nakamura T, Komori M, Kawai N, Nishihara A, Nakanishi F, Nakahara M, Ogiyama H, Kinoshita K, Yamada T, Iijima H, Tsujii M, Takehara T. Scheduled endoscopic surveillance controls secondary cancer after curative endoscopic resection for early gastric cancer: a multicentre retrospective cohort study by Osaka University ESD study group. Gut 2013; 62: 1425-1432 [PMID: 22914298 DOI: 10.1136/gutjnl-2011-301647]
52. 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 Pathol Microbiol Scand 1965; 64: 31-49 [PMID: 14320675]
53. Correa P, Fox J, Fontham E, Ruiz B, Lin YP, Zavala D, Taylor N, Mackinley D, de Lima E, Portilla H. Helicobacter pylori and gastric carcinoma. Serum antibody prevalence in populations with contrasting cancer risks. Cancer 1990; 66: 2569-2574 [PMID: 2249197]
54. Sipponen P, Hyvärinen H. Role of Helicobacter pylori in the pathogenesis of gastritis, peptic ulcer and gastric cancer. Scand J Gastroenterol Suppl 1993; 196: 3-6 [PMID: 8341988]
55. Kikuchi S, Wada O, Nakajima T, Nishi T, Kobayashi O, Konishi T, Inaba Y. Serum anti-Helicobacter pylori antibody and gastric carcinoma among young adults. Research Group on Prevention of Gastric Carcinoma among Young Adults. Cancer 1995; 75: 2789-2793 [PMID: 7773928]
56. Kokkola A, Valle J, Haapiainen R, Sipponen P, Kivilaakso E, Puolakkainen P. Helicobacter pylori infection in young patients with gastric carcinoma. Scand J Gastroenterol 1996; 31: 643-647 [PMID: 8819211]
57. Tanaka A, Watari J, Tanabe H, Maemoto A, Fujiya M, Ashida T, KM D, Kohgo Y. Effect of eradication of Helicobacter pylori on genetic instabilities in gastric intestinal metaplasia. Aliment Pharmacol Ther 2006; 24 Suppl 4: 194-202
58. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, Taniyama K, Sasaki N, Schlemper RJ. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 2001; 345: 784-789 [PMID: 11556297 DOI: 10.1056/NEJMoa001999]
59. Kamangar F, Dawsey SM, Blaser MJ, Perez-Perez GI, Pietinen P, Newschaffer CJ, Abnet CC, Albanes D, Virtamo J, Taylor PR. Opposing risks of gastric cardia and noncardia gastric adenocarcinomas associated with Helicobacter pylori seropositivity. J Natl Cancer Inst 2006; 98: 1445-1452 [PMID: 17047193 DOI: 10.1093/jnci/djj393]
60. Graham DY, Lu H, Yamaoka Y. African, Asian or Indian enigma, the East Asian Helicobacter pylori: facts or medical myths. J Dig Dis 2009; 10: 77-84 [PMID: 19426388 DOI: 10.1111/j.1751-2980.2009.00368.x]
61. Miwa H, Go MF, Sato N. H. pylori and gastric cancer: the Asian enigma. Am J Gastroenterol 2002; 97: 1106-1112 [PMID: 12014714 DOI: 10.1111/j.1572-0241.2002.05663.x]
62. Goh KL. Epidemiology of Helicobacter pylori infection in Malaysia--observations in a multiracial Asian population. Med J Malaysia 2009; 64: 187-192 [PMID: 20527265]
63. Huang JQ, Zheng GF, Sumanac K, Irvine EJ, Hunt RH. Meta-analysis of the relationship between cagA seropositivity and gastric cancer. Gastroenterology 2003; 125: 1636-1644 [PMID: 14724815]
64. Correa P, Piazuelo MB. The gastric precancerous cascade. J Dig Dis 2012; 13: 2-9 [PMID: 22188910 DOI: 10.1111/ j.1751-2980.2011.00550.x]
65. Ito Y, Azuma T, Ito S, Miyaji H, Hirai M, Yamazaki Y, Sato F, Kato T, Kohli Y, Kuriyama M. Analysis and typing of the vacA gene from cagA-positive strains of Helicobacter pylori isolated in Japan. J Clin Microbiol 1997; 35: 1710-1714 [PMID: 9196179]
66. Maeda S, Ogura K, Yoshida H, Kanai F, Ikenoue T, Kato N, Shiratori Y, Omata M. Major virulence factors, VacA and CagA, are commonly positive in Helicobacter pylori isolates in Japan. Gut 1998; 42: 338-343 [PMID: 9577338]
67. Yamaoka Y, Souchek J, Odenbreit S, Haas R, Arnqvist A, Borén T, Kodama T, Osato MS, Gutierrez O, Kim JG, Graham DY. Discrimination between cases of duodenal ulcer and gastritis on the basis of putative virulence factors of Helicobacter pylori. J Clin Microbiol 2002; 40: 2244-2246 [PMID: 12037098]
68. González CA, Figueiredo C, Lic CB, Ferreira RM, Pardo ML, Ruiz Liso JM, Alonso P, Sala N, Capella G, Sanz-Anquela JM. Helicobacter pylori cagA and vacA genotypes as predictors of progression of gastric preneoplastic lesions: a long-term follow-up in a high-risk area in Spain. Am J Gastroenterol 2011; 106: 867-874 [PMID: 21285949 DOI: 10.1038/ajg.2011.1]
69. Wang HJ, Kuo CH, Yeh AA, Chang PC, Wang WC. Vacuolating toxin production in clinical isolates of Helicobacter pylori with different vacA genotypes. J Infect Dis 1998; 178: 207-212 [PMID: 9652442]
70. Mukhopadhyay AK, Kersulyte D, Jeong JY, Datta S, Ito Y, Chowdhury A, Chowdhury S, Santra A, Bhattacharya SK, Azuma T, Nair GB, Berg DE. Distinctiveness of genotypes of Helicobacter pylori in Calcutta, India. J Bacteriol 2000; 182: 3219-3227 [PMID: 10809703]
71. Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol 1996; 20: 1161-1181 [PMID: 8827022]
72. Lechago J, Correa P. Prolonged achlorhydria and gastric neoplasia: is there a causal relationship? Gastroenterology 1993; 104: 1554-1557 [PMID: 8482469]
73. de Vries AC, Haringsma J, Kuipers EJ. The detection, surveillance and treatment of premalignant gastric lesions related to Helicobacter pylori infection. Helicobacter 2007; 12: 1-15 [PMID: 17241295 DOI: 10.1111/j.1523-5378.2007.00475. x]
74. Kim N, Park YS, Cho SI, Lee HS, Choe G, Kim IW, Won YD, Park JH, Kim JS, Jung HC, Song IS. Prevalence and risk factors of atrophic gastritis and intestinal metaplasia in a Korean population without significant gastroduodenal disease. Helicobacter 2008; 13: 245-255 [PMID: 18665932 DOI: 10.1111/j.1523-5378.2008.00604.x]
75. Sipponen P, Kekki M, Haapakoski J, Ihamäki T, Siurala M. Gastric cancer risk in chronic atrophic gastritis: statistical calculations of cross-sectional data. Int J Cancer 1985; 35: 173-177 [PMID: 3871738]
76. Mera R, Fontham ET, Bravo LE, Bravo JC, Piazuelo MB, Camargo MC, Correa P. Long term follow up of patients treated for Helicobacter pylori infection. Gut 2005; 54: 1536-1540 [PMID: 15985559 DOI: 10.1136/gut.2005.072009]
77. Take S, Mizuno M, Ishiki K, Nagahara Y, Yoshida T, Yokota K, Oguma K, Okada H, Shiratori Y. The effect of eradicating helicobacter pylori on the development of gastric cancer in patients with peptic ulcer disease. Am J Gastroenterol 2005; 100: 1037-1042 [PMID: 15842576 DOI: 10.1111/ j.1572-0241.2005.41384.x]
78. Miki K, Ichinose M, Shimizu A, Huang SC, Oka H, Furihata C, Matsushima T, Takahashi K. Serum pepsinogens as a screening test of extensive chronic gastritis. Gastroenterol Jpn 1987; 22: 133-141 [PMID: 3596151]
79. Ichinose M, Yahagi N, Oka M, Ikeda H, Miki K, Omata M. Screening for gastric cancer in Japan. In: Wu GY, Aziz K, editors. Cancer screening for common malignancies. Totowa, New Jersey: Humana Press 2001: 87-102.
80. Watanabe Y, Kurata JH, Mizuno S, Mukai M, Inokuchi H, Miki K, Ozasa K, Kawai K. Helicobacter pylori infection and gastric cancer. A nested case-control study in a rural area of Japan. Dig Dis Sci 1997; 42: 1383-1387 [PMID: 9246033]
81. Dinis-Ribeiro M, Yamaki G, Miki K, Costa-Pereira A, Matsukawa M, Kurihara M. Meta-analysis on the validity of pepsinogen test for gastric carcinoma, dysplasia or chronic atrophic gastritis screening. J Med Screen 2004; 11: 141-147 [PMID: 15333273 DOI: 10.1258/0969141041732184]
82. Ohata H, Kitauchi S, Yoshimura N, Mugitani K, Iwane M, Nakamura H, Yoshikawa A, Yanaoka K, Arii K, Tamai H, Shimizu Y, Takeshita T, Mohara O, Ichinose M. Progression of chronic atrophic gastritis associated with Helicobacter pylori infection increases risk of gastric cancer. Int J Cancer 2004; 109: 138-143 [PMID: 14735480 DOI: 10.1002/ijc.11680]
83. Yanaoka K, Oka M, Yoshimura N, Mukoubayashi C, Enomoto S, Iguchi M, Magari H, Utsunomiya H, Tamai H, Arii K, Yamamichi N, Fujishiro M, Takeshita T, Mohara O, Ichinose M. Risk of gastric cancer in asymptomatic, middle-aged Japanese subjects based on serum pepsinogen and Helicobacter pylori antibody levels. Int J Cancer 2008; 123: 917-926 [PMID: 18508314 DOI: 10.1002/ijc.23571]
84. Rugge M, Genta RM. Staging gastritis: an international proposal. Gastroenterology 2005; 129: 1807-1808 [PMID: 16285989 DOI: 10.1053/j.gastro.2005.09.056]
85. Rugge M, Genta RM. Staging and grading of chronic gastritis. Hum Pathol 2005; 36: 228-233 [PMID: 15791566 DOI: 10.1016/j.humpath.2004.12.008]
86. Rugge M, Meggio A, Pennelli G, Piscioli F, Giacomelli L, De Pretis G, Graham DY. Gastritis staging in clinical practice: the OLGA staging system. Gut 2007; 56: 631-636 [PMID: 17142647 DOI: 10.1136/gut.2006.106666]
87. Satoh K, Osawa H, Yoshizawa M, Nakano H, Hirasawa T, Kihira K, Sugano K. Assessment of atrophic gastritis using the OLGA system. Helicobacter 2008; 13: 225-229 [PMID: 18466398 DOI: 10.1111/j.1523-5378.2008.00599.x]
88. Rugge M, de Boni M, Pennelli G, de Bona M, Giacomelli L, Fassan M, Basso D, Plebani M, Graham DY. Gastritis OLGA-staging and gastric cancer risk: a twelve-year clinico-pathological follow-up study. Aliment Pharmacol Ther 2010; 31: 1104-1111 [PMID: 20180784 DOI: 10.1111/ j.1365-2036.2010.04277.x]
89. Sipponen P, Stolte M. Clinical impact of routine biopsies of the gastric antrum and body. Endoscopy 1997; 29: 671-678 [PMID: 9360882 DOI: 10.1055/s-2007-1004278]
90. Garcia SB, Park HS, Novelli M, Wright NA. Field cancerization, clonality, and epithelial stem cells: the spread of mutated clones in epithelial sheets. J Pathol 1999; 187: 61-81 [PMID: 10341707 DOI: 10.1002/(sici)1096-9896(199901)187:1<61:: aid-path247>3.0.co;2-i]
91. Filipe MI, Muñoz N, Matko I, Kato I, Pompe-Kirn V, Jutersek A, Teuchmann S, Benz M, Prijon T. Intestinal metaplasia types and the risk of gastric cancer: a cohort study in Slovenia. Int J Cancer 1994; 57: 324-329 [PMID: 8168991]
92. Filipe MI, Jass J. Intestinal metaplasia subtypes and cancer risk. In: Filipe MI, Jass JR, editors. Gastric carcinoma. Edinburgh: Churchill Livingston, 1986: 212-236
93. González CA, Pardo ML, Liso JM, Alonso P, Bonet C, Garcia RM, Sala N, Capella G, Sanz-Anquela JM. Gastric cancer occurrence in preneoplastic lesions: a long-term follow-up in a high-risk area in Spain. Int J Cancer 2010; 127: 2654-2660 [PMID: 20178099 DOI: 10.1002/ijc.25273]
94. Rokkas T, Filipe MI, Sladen GE. Detection of an increased incidence of early gastric cancer in patients with intestinal metaplasia type III who are closely followed up. Gut 1991; 32: 1110-1113 [PMID: 1955163]
95. Shiotani A, Haruma K, Uedo N, Iishi H, Ishihara R, Tatsuta M, Kumamoto M, Nakae Y, Ishiguro S, Graham DY. Histological risk markers for non-cardia early gastric cancer. Pattern of mucin expression and gastric cancer. Virchows Arch 2006; 449: 652-659 [PMID: 17058096 DOI: 10.1007/ s00428-006-0300-8]
96. Ectors N, Dixon MF. The prognostic value of sulphomucin positive intestinal metaplasia in the development of gastric cancer. Histopathology 1986; 10: 1271-1277 [PMID: 3817762]
97. Ramesar KC, Sanders DS, Hopwood D. Limited value of type III intestinal metaplasia in predicting risk of gastric carcinoma. J Clin Pathol 1987; 40: 1287-1290 [PMID: 3693566]
98. El-Zimaity HM, Ramchatesingh J, Saeed MA, Graham DY. Gastric intestinal metaplasia: subtypes and natural history. J Clin Pathol 2001; 54: 679-683 [PMID: 11533073]
99. Tosi P, Filipe MI, Luzi P, Miracco C, Santopietro R, Lio R, Sforza V, Barbini P. Gastric intestinal metaplasia type III cases are classified as low-grade dysplasia on the basis of morphometry. J Pathol 1993; 169: 73-78 [PMID: 8433217 DOI: 10.1002/path.1711690112]
100. Matsukuma A, Mori M, Enjoji M. Sulphomucin-secreting intestinal metaplasia in the human gastric mucosa. An association with intestinal-type gastric carcinoma. Cancer 1990; 66: 689-694 [PMID: 2386900]
101. Antonioli DA. Precursors of gastric carcinoma: a critical review with a brief description of early (curable) gastric cancer. Hum Pathol 1994; 25: 994-1005 [PMID: 7927322]
102. Sasaki I, Yao T, Nawata H, Tsuneyoshi M. Minute gastric carcinoma of differentiated type with special reference to the significance of intestinal metaplasia, proliferative zone, and p53 protein during tumor development. Cancer 1999; 85: 1719-1729 [PMID: 10223565]
103. Leung WK, Sung JJ. Review article: intestinal metaplasia and gastric carcinogenesis. Aliment Pharmacol Ther 2002; 16: 1209-1216 [PMID: 12144569]
104. Sun JH, Das KK, Amenta PS, Yokota K, Watari J, Sato T, Kohgo Y, Das KM. Preferential expression of cyclooxygenase-2 in colonic-phenotype of gastric intestinal metaplasia: association with helicobacter pylori and gastric carcinoma. J Clin Gastroenterol 2006; 40: 122-128 [PMID: 16394872]
105. Das KM, Sakamaki S, Vecchi M, Diamond B. The production and characterization of monoclonal antibodies to a human colonic antigen associated with ulcerative colitis: cellular localization of the antigen by using the monoclonal antibody. J Immunol 1987; 139: 77-84 [PMID: 3295053]
106. Mirza ZK, Das KK, Slate J, Mapitigama RN, Amenta PS, Griffel LH, Ramsundar L, Watari J, Yokota K, Tanabe H, Sato T, Kohgo Y, Das KM. Gastric intestinal metaplasia as detected by a monoclonal antibody is highly associated with gastric adenocarcinoma. Gut 2003; 52: 807-812 [PMID: 12740335]
107. Watari J, Das KK, Amenta PS, Tanabe H, Tanaka A, Geng X, Lin JJ, Kohgo Y, Das KM. Effect of eradication of Helicobacter pylori on the histology and cellular phenotype of gastric intestinal metaplasia. Clin Gastroenterol Hepatol 2008; 6: 409-417 [PMID: 18321787 DOI: 10.1016/j.cgh.2007.12.044]
108. Leung WK, Kim JJ, Kim JG, Graham DY, Sepulveda AR. Microsatellite instability in gastric intestinal metaplasia in patients with and without gastric cancer. Am J Pathol 2000; 156: 537-543 [PMID: 10666383 DOI: 10.1016/s0002-9440(10)64758-x]
109. Liu P, Zhang XY, Shao Y, Zhang DF. Microsatellite instability in gastric cancer and pre-cancerous lesions. World J Gastroenterol 2005; 11: 4904-4907 [PMID: 16097069]
110. Kashiwagi K, Watanabe M, Ezaki T, Kanai T, Ishii H, Mukai M, Hibi T. Clinical usefulness of microsatellite instability for the prediction of gastric adenoma or adenocarcinoma in patients with chronic gastritis. Br J Cancer 2000; 82: 1814-1818 [PMID: 10839296 DOI: 10.1054/bjoc.1999.1154]
111. Jin Z, Tamura G, Satoh M, Meguro T, Miura T, Hayashi M, Osakabe M, Ohmura K, Ogata S, Endoh Y, Motoyama T. Absence of BAT-26 instability in gastric intestinal metaplasia. Pathol Int 2001; 51: 473-475 [PMID: 11422810]
112. Zaky AH, Watari J, Tanabe H, Sato R, Moriichi K, Tanaka A, Maemoto A, Fujiya M, Ashida T, Kohgo Y. Clinicopathologic implications of genetic instability in intestinal-type gastric cancer and intestinal metaplasia as a precancerous lesion: proof of field cancerization in the stomach. Am J Clin Pathol 2008; 129: 613-621 [PMID: 18343789 DOI: 10.1309/dflelpgpnv5lk6b1]
113. Watari J, Moriichi K, Tanabe H, Kashima S, Nomura Y, Fujiya M, Tomita T, Oshima T, Fukui H, Miwa H, Das KM, Kohgo Y. Biomarkers predicting development of metachronous gastric cancer after endoscopic resection: an analysis of molecular pathology of Helicobacter pylori eradication. Int J Cancer 2012; 130: 2349-2358 [PMID: 21732341 DOI: 10.1002/ ijc.26275]
114. Suh E, Traber PG. An intestine-specific homeobox gene regulates proliferation and differentiation. Mol Cell Biol 1996; 16: 619-625 [PMID: 8552090]
115. Soubeyran P, André F, Lissitzky JC, Mallo GV, Moucadel V, Roccabianca M, Rechreche H, Marvaldi J, Dikic I, Dagorn JC, Iovanna JL. Cdx1 promotes differentiation in a rat intestinal epithelial cell line. Gastroenterology 1999; 117: 1326-1338 [PMID: 10579974]
116. Satoh K, Mutoh H, Eda A, Yanaka I, Osawa H, Honda S, Kawata H, Kihira K, Sugano K. Aberrant expression of CDX2 in the gastric mucosa with and without intestinal metaplasia: effect of eradication of Helicobacter pylori. Helicobacter 2002; 7: 192-198 [PMID: 12047325]
117. Mutoh H, Hakamata Y, Sato K, Eda A, Yanaka I, Honda S, Osawa H, Kaneko Y, Sugano K. Conversion of gastric mucosa to intestinal metaplasia in Cdx2-expressing transgenic mice. Biochem Biophys Res Commun 2002; 294: 470-479 [PMID: 12051735 DOI: 10.1016/s0006-291x(02)00480-1]
118. Mutoh H, Sakurai S, Satoh K, Tamada K, Kita H, Osawa H, Tomiyama T, Sato Y, Yamamoto H, Isoda N, Yoshida T, Ido K, Sugano K. Development of gastric carcinoma from intestinal metaplasia in Cdx2-transgenic mice. Cancer Res 2004; 64: 7740-7747 [PMID: 15520178 DOI: 10.1158/0008-5472. can-04-1617]
119. Gong C, Mera R, Bravo JC, Ruiz B, Diaz-Escamilla R, Fontham ET, Correa P, Hunt JD. KRAS mutations predict progression of preneoplastic gastric lesions. Cancer Epidemiol Biomarkers Prev 1999; 8: 167-171 [PMID: 10067815]
120. Hiyama T, Haruma K, Kitadai Y, Masuda H, Miyamoto M, Tanaka S, Yoshihara M, Shimamoto F, Chayama K. K-ras mutation in helicobacter pylori-associated chronic gastritis in patients with and without gastric cancer. Int J Cancer 2002; 97: 562-566 [PMID: 11807778]
121. Watari J, Tanaka A, Tanabe H, Sato R, Moriichi K, Zaky A, Okamoto K, Maemoto A, Fujiya M, Ashida T, Das KM, Kohgo Y. K-ras mutations and cell kinetics in Helicobacter pylori associated gastric intestinal metaplasia: a comparison before and after eradication in patients with chronic gastritis and gastric cancer. J Clin Pathol 2007; 60: 921-926 [PMID: 16997920 DOI: 10.1136/jcp.2006.041939]
122. Ushijima T, Sasako M. Focus on gastric cancer. Cancer Cell 2004; 5: 121-125 [PMID: 14998488]
123. Herman JG, Umar A, Polyak K, Graff JR, Ahuja N, Issa JP, Markowitz S, Willson JK, Hamilton SR, Kinzler KW, Kane MF, Kolodner RD, Vogelstein B, Kunkel TA, Baylin SB. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci USA 1998; 95: 6870-6875 [PMID: 9618505]
124. Fleisher AS, Esteller M, Tamura G, Rashid A, Stine OC, Yin J, Zou TT, Abraham JM, Kong D, Nishizuka S, James SP, Wilson KT, Herman JG, Meltzer SJ. Hypermethylation of the hMLH1 gene promoter is associated with microsatellite instability in early human gastric neoplasia. Oncogene 2001; 20: 329-335 [PMID: 11313962 DOI: 10.1038/sj.onc.1204104]
125. Maekita T, Nakazawa K, Mihara M, Nakajima T, Yanaoka K, Iguchi M, Arii K, Kaneda A, Tsukamoto T, Tatematsu M, Tamura G, Saito D, Sugimura T, Ichinose M, Ushijima T. High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk. Clin Cancer Res 2006; 12: 989-995 [PMID: 16467114 DOI: 10.1158/1078-0432.ccr-05-2096]
126. Enomoto S, Maekita T, Tsukamoto T, Nakajima T, Nakazawa K, Tatematsu M, Ichinose M, Ushijima T. Lack of association between CpG island methylator phenotype in human gastric cancers and methylation in their background noncancerous gastric mucosae. Cancer Sci 2007; 98: 1853-1861 [PMID: 17900260 DOI: 10.1111/j.1349-7006.2007.00625.x]
127. Nakajima T, Yamashita S, Maekita T, Niwa T, Nakazawa K, Ushijima T. The presence of a methylation fingerprint of Helicobacter pylori infection in human gastric mucosae. Int J Cancer 2009; 124: 905-910 [PMID: 19035455 DOI: 10.1002/ ijc.24018]
128. Chan AO, Lam SK, Wong BC, Kwong YL, Rashid A. Gene methylation in non-neoplastic mucosa of gastric cancer: age or Helicobacter pylori related? Am J Pathol 2003; 163: 370-31; author reply 370-31; [PMID: 12819044]
129. Forbes GM, Warren JR, Glaser ME, Cullen DJ, Marshall BJ, Collins BJ. Long-term follow-up of gastric histology after Helicobacter pylori eradication. J Gastroenterol Hepatol 1996; 11: 670-673 [PMID: 8840244]
130. Ito M, Haruma K, Kamada T, Mihara M, Kim S, Kitadai Y, Sumii M, Tanaka S, Yoshihara M, Chayama K. Helicobacter pylori eradication therapy improves atrophic gastritis and intestinal metaplasia: a 5-year prospective study of patients with atrophic gastritis. Aliment Pharmacol Ther 2002; 16: 1449-1456 [PMID: 12182744]
131. Zhou L, Sung JJ, Lin S, Jin Z, Ding S, Huang X, Xia Z, Guo H, Liu J, Chao W. A five-year follow-up study on the pathological changes of gastric mucosa after H. pylori eradication. Chin Med J (Engl) 2003; 116: 11-14 [PMID: 12667379]
132. Leung WK, Lin SR, Ching JY, To KF, Ng EK, Chan FK, Lau JY, Sung JJ. Factors predicting progression of gastric intestinal metaplasia: results of a randomised trial on Helicobacter pylori eradication. Gut 2004; 53: 1244-1249 [PMID: 15306578 DOI: 10.1136/gut.2003.034629]
133. Vannella L, Lahner E, Bordi C, Pilozzi E, Di Giulio E, Corleto VD, Osborn J, Delle Fave G, Annibale B. Reversal of atrophic body gastritis after H. pylori eradication at long-term follow-up. Dig Liver Dis 2011; 43: 295-299 [PMID: 21112822 DOI: 10.1016/j.dld.2010.10.012]
134. Kodama M, Murakami K, Okimoto T, Sato R, Uchida M, Abe T, Shiota S, Nakagawa Y, Mizukami K, Fujioka T. Ten-year prospective follow-up of histological changes at five points on the gastric mucosa as recommended by the updated Sydney system after Helicobacter pylori eradication. J Gastroenterol 2012; 47: 394-403 [PMID: 22138891 DOI: 10.1007/s00535-011-0504-9]
135. Rokkas T, Pistiolas D, Sechopoulos P, Robotis I, Margantinis G. The long-term impact of Helicobacter pylori eradication on gastric histology: a systematic review and meta-analysis. Helicobacter 2007; 12 Suppl 2: 32-38 [PMID: 17991174 DOI: 10.1111/j.1523-5378.2007.00563.x]
136. Wang J, Xu L, Shi R, Huang X, Li SW, Huang Z, Zhang G. Gastric atrophy and intestinal metaplasia before and after Helicobacter pylori eradication: a meta-analysis. Digestion 2011; 83: 253-260 [PMID: 21282951 DOI: 10.1159/000280318]
137. Lin JL, Geng X, Bhattacharya SD, Yu JR, Reiter RS, Sastri B, Glazier KD, Mirza ZK, Wang KK, Amenta PS, Das KM, Lin JJ. Isolation and sequencing of a novel tropomyosin isoform preferentially associated with colon cancer. Gastroenterology 2002; 123: 152-162 [PMID: 12105844]
138. Chan AO, Peng JZ, Lam SK, Lai KC, Yuen MF, Cheung HK, Kwong YL, Rashid A, Chan CK, Wong BC. Eradication of Helicobacter pylori infection reverses E-cadherin promoter hypermethylation. Gut 2006; 55: 463-468 [PMID: 16428266 DOI: 10.1136/gut.2005.077776]
139. Leung WK, Man EP, Yu J, Go MY, To KF, Yamaoka Y, Cheng VY, Ng EK, Sung JJ. Effects of Helicobacter pylori eradication on methylation status of E-cadherin gene in noncancerous stomach. Clin Cancer Res 2006; 12: 3216-3221 [PMID: 16707623 DOI: 10.1158/1078-0432.ccr-05-2442]
140. Nakajima T, Enomoto S, Yamashita S, Ando T, Nakanishi Y, Nakazawa K, Oda I, Gotoda T, Ushijima T. Persistence of a component of DNA methylation in gastric mucosae after Helicobacter pylori eradication. J Gastroenterol 2010; 45: 37-44 [PMID: 19821005 DOI: 10.1007/s00535-009-0142-7]
141. Enomoto S, Maekita T, Ohata H, Yanaoka K, Oka M, Ichinose M. Novel risk markers for gastric cancer screening: Present status and future prospects. World J Gastrointest Endosc 2010; 2: 381-387 [PMID: 21191511 DOI: 10.4253/wjge.v2.i12.381]
142. Ito M, Takata S, Tatsugami M, Wada Y, Imagawa S, Matsumoto Y, Takamura A, Kitamura S, Matsuo T, Tanaka S, Haruma K, Chayama K. Clinical prevention of gastric cancer by Helicobacter pylori eradication therapy: a systematic review. J Gastroenterol 2009; 44: 365-371 [PMID: 19333542 DOI: 10.1007/s00535-009-0036-8]
143. Wong BC, Lam SK, Wong WM, Chen JS, Zheng TT, Feng RE, Lai KC, Hu WH, Yuen ST, Leung SY, Fong DY, Ho J, Ching CK, Chen JS. Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA 2004; 291: 187-194 [PMID: 14722144 DOI: 10.1001/jama.291.2.187]
144. Wright CL, Kelly JK. The use of routine special stains for upper gastrointestinal biopsies. Am J Surg Pathol 2006; 30: 357-361 [PMID: 16538056 DOI: 10.1097/01.pas.0000184808.45661.cb]
145. Uemura N, Mukai T, Okamoto S, Yamaguchi S, Mashiba H, Taniyama K, Sasaki N, Haruma K, Sumii K, Kajiyama G. Effect of Helicobacter pylori eradication on subsequent development of cancer after endoscopic resection of early gastric cancer. Cancer Epidemiol Biomarkers Prev 1997; 6: 639-642 [PMID: 9264278]
146. de Vries AC, Meijer GA, Looman CW, Casparie MK, Hansen BE, van Grieken NC, Kuipers EJ. Epidemiological trends of pre-malignant gastric lesions: a long-term nationwide study in the Netherlands. Gut 2007; 56: 1665-1670 [PMID: 17698860 DOI: 10.1136/gut.2007.127167]
147. Wu CY, Kuo KN, Wu MS, Chen YJ, Wang CB, Lin JT. Early Helicobacter pylori eradication decreases risk of gastric cancer in patients with peptic ulcer disease. Gastroenterology 2009; 137: 1641-8. e1-2 [PMID: 19664631 DOI: 10.1053/ j.gastro.2009.07.060]
148. de Vries AC, van Grieken NC, Looman CW, Casparie MK, de Vries E, Meijer GA, Kuipers EJ. Gastric cancer risk in patients with premalignant gastric lesions: a nationwide cohort study in the Netherlands. Gastroenterology 2008; 134: 945-952 [PMID: 18395075 DOI: 10.1053/j.gastro.2008.01.071]
149. Areia M, Carvalho R, Cadime AT, Rocha Gonçalves F, Dinis-Ribeiro M. Screening for gastric cancer and surveillance of premalignant lesions: a systematic review of costeffectiveness studies. Helicobacter 2013; 18: 325-337 [PMID: 23566268 DOI: 10.1111/hel.12050]