Korean J Gastroenterol.  2016 Jun;67(6):289-299. 10.4166/kjg.2016.67.6.289.

Peptic Ulcer Disease Associated with Helicobacter pylori Infection

• Yeo SH
• Yang CH

• KMID: 2307755
• DOI: http://doi.org/10.4166/kjg.2016.67.6.289

Abstract

Although the global prevalence of peptic ulcer disease (PUD) is decreasing, PUD is still one of the most common upper gastrointestinal diseases in the world due to Helicobacter pylori infection and increased use of non-steroidal anti-inflammatory drugs. In Korea, the prevalence of H. pylori infection is also declining, but it is still the major cause of PUD. The outcomes of H. pylori infection are caused by imbalances between bacterial virulence factors, host factors, and environmental influences. In this review, we describe the prevalence trends of H. pylori infection in Korea, the mechanism of H. pylori infection-related PUD, and treatment strategies.

Keyword

Helicobacter pylori; Peptic ulcer; Prevalence; Epidemiology; Therapy

MeSH Terms

Epidemiology
Gastrointestinal Diseases
Helicobacter pylori*
Helicobacter*
Korea
Peptic Ulcer*
Prevalence
Virulence Factors
Virulence Factors

Figure

• 

  Fig. 1. Trends of seroprevalence of Helicobacter pylori infection in asymptomatic subjects without a history of H. pylori eradication in 1998, 2005, and 2011 (*p<0.05). Seroprevalence by sex (A), by geographic area (B) and by age (C).18

Reference

References

1. Graham DY. Helicobacter pylori: its epidemiology and its role in duodenal ulcer disease. J Gastroenterol Hepatol. 1991; 6:105–113.

2. Wotherspoon AC, Ortiz-Hidalgo C, Falzon MR, Isaacson PG. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet. 1991; 338:1175–1176.

3. Parsonnet J. Helicobacter pylori and gastric cancer. Gastroenterol Clin North Am. 1993; 22:89–104.

4. Ford AC, Delaney BC, Forman D, Moayyedi P. Eradication therapy for peptic ulcer disease in Helicobacter pylori positive patients. Cochrane Database Syst Rev. 2006; 4:CD003840.

5. Hentschel E, Brandstätter G, Dragosics B, et al. Effect of ranitidine and amoxicillin plus metronidazole on the eradication of Helicobacter pylori and the recurrence of duodenal ulcer. N Engl J Med. 1993; 328:308–312.

6. Miwa H, Sakaki N, Sugano K, et al. Recurrent peptic ulcers in patients following successful Helicobacter pylori eradication: a multicenter study of 4940 patients. Helicobacter. 2004; 9:9–16.

7. Kim SG, Jung HK, Lee HL, et al. Korean College of Helicobacter and Upper Gastrointestinal Research. Guidelines for the diagnosis and treatment of Helicobacter pylori infection in Korea, 2013 revised edition. Korean J Gastroenterol. 2013; 62:3–26.

8. Malfertheiner P, Megraud F, O'Morain CA, et al. European Helicobacter Study Group. Management of Helicobacter pylori infection–the Maastricht IV/Florence Consensus Report. Gut. 2012; 61:646–664.

9. de Jesus NZ, de Souza Falcão H, Gomes IF, et al. Tannins, peptic ulcers and related mechanisms. Int J Mol Sci. 2012; 13:3203–3228.

10. Pérez-Aisa MA, Del Pino D, Siles M, Lanas A. Clinical trends in ulcer diagnosis in a population with high prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther. 2005; 21:65–72.

11. García Rodríguez LA, Hernández-Díaz S. Risk of uncomplicated peptic ulcer among users of aspirin and nonaspirin nonsteroidal antiinflammatory drugs. Am J Epidemiol. 2004; 159:23–31.

12. Kurata JH, Nogawa AN. Meta-analysis of risk factors for peptic ulcer. Nonsteroidal antiinflammatory drugs, Helicobacter pylori, and smoking. J Clin Gastroenterol. 1997; 24:2–17.

13. Leong RW. Differences in peptic ulcer between the East and the West. Gastroenterol Clin North Am. 2009; 38:363–379.

14. Fujisawa T, Kumagai T, Akamatsu T, Kiyosawa K, Matsunaga Y. Changes in seroepidemiological pattern of Helicobacter pylori and hepatitis A virus over the last 20 years in Japan. Am J Gastroenterol. 1999; 94:2094–2099.

15. Chen J, Bu XL, Wang QY, Hu PJ, Chen MH. Decreasing seroprevalence of Helicobacter pylori infection during 1993–2003 in Guangzhou, southern China. Helicobacter. 2007; 12:164–169.

16. Kim JH, Kim HY, Kim NY, et al. Korea H pylori Study Group, South Korea. Seroepidemiological study of Helicobacter pylori infection in asymptomatic people in South Korea. J Gastroenterol Hepatol. 2001; 16:969–975.

17. Yim JY, Kim N, Choi SH, et al. Seroprevalence of Helicobacter pylori in South Korea. Helicobacter. 2007; 12:333–340.

18. Lim SH, Kwon JW, Kim N, et al. Prevalence and risk factors of Helicobacter pylori infection in Korea: nationwide multicenter study over 13 years. BMC Gastroenterol. 2013; 13:104.

19. Valle J, Kekki M, Sipponen P, Ihamäki T, Siurala M. Longterm course and consequences of Helicobacter pylori gastritis. Results of a 32-year follow-up study. Scand J Gastroenterol. 1996; 31:546–550.

20. Brown LM. Helicobacter pylori: epidemiology and routes of transmission. Epidemiol Rev. 2000; 22:283–297.

21. Kignel S, de Almeida Pina F, André EA, Alves Mayer MP, Birman EG. Occurrence of Helicobacter pylori in dental plaque and saliva of dyspeptic patients. Oral Dis. 2005; 11:17–21.

22. Bui D, Brown HE, Harris RB, Oren E. Serologic evidence for fecal-oral transmission of Helicobacter pylori. Am J Trop Med Hyg. 2016; 94:82–88.

23. Navabi N, Aramon M, Mirzazadeh A. Does the presence of the Helicobacter pylori in the dental plaque associate with its gastric infection? A metaanalysis and systematic review. Dent Res J (Isfahan). 2011; 8:178–182.

24. Drumm B, Perez-Perez GI, Blaser MJ, Sherman PM. Intrafamilial clustering of Helicobacter pylori infection. N Engl J Med. 1990; 322:359–363.

25. Brenner H, Weyermann M, Rothenbacher D. Clustering of Helicobacter pylori infection in couples: differences between high- and low-prevalence population groups. Ann Epidemiol. 2006; 16:516–520.

26. Sari YS, Can D, Tunali V, Sahin O, Koc O, Bender O. H pylori: Treatment for the patient only or the whole family? World J Gastroenterol. 2008; 14:1244–1247.

27. Krueger WS, Hilborn ED, Converse RR, Wade TJ. Environmental risk factors associated with Helicobacter pylori seroprevalence in the United States: a cross-sectional analysis of NHANES data. Epidemiol Infect. 2015; 143:2520–2531.

28. Bartholomeeusen S, Vandenbroucke J, Truyers C, Buntinx F. Time trends in the incidence of peptic ulcers and oesophagitis between 1994 and 2003. Br J Gen Pract. 2007; 57:497–499.

29. el-Serag HB, Sonnenberg A. Opposing time trends of peptic ulcer and reflux disease. Gut. 1998; 43:327–333.

30. Manuel D, Cutler A, Goldstein J, Fennerty MB, Brown K. Decreasing prevalence combined with increasing eradication of Helicobacter pylori infection in the United States has not resulted in fewer hospital admissions for peptic ulcer disease-related complications. Aliment Pharmacol Ther. 2007; 25:1423–1427.

31. Kim N, Kim JW, Kim HJ, et al. Distribution of upper gastroduodenal diseases in health check-up subjects in 2006. Korean J Helicobacter Up Gastroinest Res. 2008; 8:1–8.

32. Kim JJ, Kim N, Park HK, et al. Clinical characteristics of patients diagnosed as peptic ulcer disease in the third referral center in 2007. Korean J Gastroenterol. 2012; 59:338–346.

33. Kim HS, Baik SJ, Kim KH, et al. Prevalence of and risk factors for gastrointestinal diseases in Korean americans and native Koreans undergoing screening endoscopy. Gut Liver. 2013; 7:539–545.

34. Kim JI, Kim SG, Kim N, et al. Korean College of Helicobacter and Upper Gastrointestinal Research. Changing prevalence of upper gastrointestinal disease in 28 893 Koreans from 1995 to 2005. Eur J Gastroenterol Hepatol. 2009; 21:787–793.

35. Chow DK, Sung JJ. Is the prevalence of idiopathic ulcers really on the increase? Nat Clin Pract Gastroenterol Hepatol. 2007; 4:176–177.

36. Kuipers EJ, Thijs JC, Festen HP. The prevalence of Helicobacter pylori in peptic ulcer disease. Aliment Pharmacol Ther. 1995; 9(Suppl 2):59–69.

37. Meucci G, Di Battista R, Abbiati C, et al. Prevalence and risk factors of Helicobacter pylori-negative peptic ulcer: a multicenter study. J Clin Gastroenterol. 2000; 31:42–47.

38. Hopkins RJ, Girardi LS, Turney EA. Relationship between Helicobacter pylori eradication and reduced duodenal and gastric ulcer recurrence: a review. Gastroenterology. 1996; 110:1244–1252.

39. Kim N, Lim SH, Lee KH, Jung HC, Song IS, Kim CY. Helicobacter pylori reinfection rate and duodenal ulcer recurrence in Korea. J Clin Gastroenterol. 1998; 27:321–326.

40. Malfertheiner P. The intriguing relationship of Helicobacter pylori infection and acid secretion in peptic ulcer disease and gastric cancer. Dig Dis. 2011; 29:459–464.

41. Go MF. Review article: natural history and epidemiology of Helicobacter pylori infection. Aliment Pharmacol Ther. 2002; 16(Suppl 1):3–15.

42. Lima VP, Silva-Fernandes IJ, Alves MK, Rabenhorst SH. Prevalence of Helicobacter pylori genotypes (vacA, cagA, cagE and virB11) in gastric cancer in Brazilian's patients: an association with histopathological parameters. Cancer Epidemiol. 2011; 35:e32–e37.

43. Gebert B, Fischer W, Weiss E, Hoffmann R, Haas R. Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science. 2003; 301:1099–1102.

44. D'Elios MM, Czinn SJ. Immunity, inflammation, and vaccines for Helicobacter pylori. Helicobacter. 2014; 19(Suppl 1):19–26.

45. Malaty HM, Graham DY. Importance of childhood socioeconomic status on the current prevalence of Helicobacter pylori infection. Gut. 1994; 35:742–745.

46. Brenner H, Rothenbacher D, Bode G, Adler G. Relation of smoking and alcohol and coffee consumption to active Helicobacter pylori infection: cross sectional study. BMJ. 1997; 315:1489–1492.

47. Barkin J. The relation between Helicobacter pylori and non-steroidal anti-inflammatory drugs. Am J Med. 1998; 105:22S–27S.

48. Papatheodoridis GV, Archimandritis AJ. Role of Helicobacter pylori eradication in aspirin or non-steroidal anti-inflammatory drug users. World J Gastroenterol. 2005; 11:3811–3816.

49. Ramsay LE, Sanmuganathan PS, Wallis EJ, Jackson PR. Aspirin for primary prevention. Treatment policy should be based on all trial evidence, not subgroup analysis. BMJ. 2000; 321:1472.

50. Lanza FL, Chan FK, Quigley EM. Practice Parameters Committee of the American College of Gastroenterology. Guidelines for prevention of NSAID-related ulcer complications. Am J Gastroenterol. 2009; 104:728–738.

51. Vergara M, Catalán M, Gisbert JP, Calvet X. Meta-analysis: role of Helicobacter pylori eradication in the prevention of peptic ulcer in NSAID users. Aliment Pharmacol Ther. 2005; 21:1411–1418.

52. Kim BG, Lee DH, Ye BD, et al. Comparison of 7-day and 14-day proton pump inhibitor-containing triple therapy for Helicobacter pylori eradication: neither treatment duration provides acceptable eradication rate in Korea. Helicobacter. 2007; 12:31–35.

53. Fuccio L, Minardi ME, Zagari RM, Grilli D, Magrini N, Bazzoli F. Meta-analysis: duration of first-line proton-pump inhibitor based triple therapy for Helicobacter pylori eradication. Ann Intern Med. 2007; 147:553–562.

54. Lee JW, Kim N, Kim JM, et al. Prevalence of primary and secondary antimicrobial resistance of Helicobacter pylori in Korea from 2003 through 2012. Helicobacter. 2013; 18:206–214.

55. Gené E, Calvet X, Azagra R, Gisbert JP. Triple vs quadruple therapy for treating Helicobacter pylori infection: an updated metaanalysis. Aliment Pharmacol Ther. 2003; 18:543–544.

56. Fischbach LA, van Zanten S, Dickason J. Meta-analysis: the efficacy, adverse events, and adherence related to first-line anti-Helicobacter pylori quadruple therapies. Aliment Pharmacol Ther. 2004; 20:1071–1082.

57. Lee HJ, Kim JI, Cheung DY, et al. Eradication of Helicobacter pylori according to 23S ribosomal RNA point mutations associated with clarithromycin resistance. J Infect Dis. 2013; 208:1123–1130.

58. Gisbert JP, Calvet X, O'Connor A, Mégraud F, O'Morain CA. Sequential therapy for Helicobacter pylori eradication: a critical review. J Clin Gastroenterol. 2010; 44:313–325.

59. Graham DY. Antibiotic resistance in Helicobacter pylori: implications for therapy. Gastroenterology. 1998; 115:1272–1277.

60. De Francesco V, Margiotta M, Zullo A, et al. Clarithromycin-resistant genotypes and eradication of Helicobacter pylori. Ann Intern Med. 2006; 144:94–100.

61. Choi HS, Chun HJ, Park SH, et al. Comparison of sequential and 7-, 10-, 14-d triple therapy for Helicobacter pylori infection. World J Gastroenterol. 2012; 18:2377–2382.

62. Chung JW, Jung YK, Kim YJ, et al. Ten-day sequential versus triple therapy for Helicobacter pylori eradication: a prospective, open-label, randomized trial. J Gastroenterol Hepatol. 2012; 27:1675–1680.

63. Kwon JH, Lee DH, Song BJ, et al. Ten-day sequential therapy as first-line treatment for Helicobacter pylori infection in Korea: a retrospective study. Helicobacter. 2010; 15:148–153.

64. Oh HS, Lee DH, Seo JY, et al. Ten-day sequential therapy is more effective than proton pump inhibitor-based therapy in Korea: a prospective, randomized study. J Gastroenterol Hepatol. 2012; 27:504–509.

65. Park HG, Jung MK, Jung JT, et al. Randomised clinical trial: a comparative study of 10-day sequential therapy with 7-day standard triple therapy for Helicobacter pylori infection in naïve patients. Aliment Pharmacol Ther. 2012; 35:56–65.

66. Kim YS, Kim SJ, Yoon JH, et al. Randomised clinical trial: the efficacy of a 10-day sequential therapy vs. a 14-day standard proton pump inhibitor-based triple therapy for Helicobacter pylori in Korea. Aliment Pharmacol Ther. 2011; 34:1098–1105.

67. Vaira D, Zullo A, Vakil N, et al. Sequential therapy versus standard triple-drug therapy for Helicobacter pylori eradication: a randomized trial. Ann Intern Med. 2007; 146:556–563.

68. Essa AS, Kramer JR, Graham DY, Treiber G. Meta-analysis: four-drug, three-antibiotic, non-bismuth-containing "concomitant therapy" versus triple therapy for Helicobacter pylori eradication. Helicobacter. 2009; 14:109–118.

69. Kim SY, Lee SW, Hyun JJ, et al. Comparative study of Helicobacter pylori eradication rates with 5-day quadruple "concomitant" therapy and 7-day standard triple therapy. J Clin Gastroenterol. 2013; 47:21–24.

70. Lim JH, Lee DH, Choi C, et al. Clinical outcomes of two-week sequential and concomitant therapies for Helicobacter pylori eradication: a randomized pilot study. Helicobacter. 2013; 18:180–186.

71. Fock KM, Katelaris P, Sugano K, et al. Second Asia-Pacific Conference. Second Asia-Pacific Consensus Guidelines for Helicobacter pylori infection. J Gastroenterol Hepatol. 2009; 24:1587–1600.

72. Lee JH, Hong SP, Kwon CI, et al. The efficacy of levofloxacin based triple therapy for Helicobacter pylori eradication. Korean J Gastroenterol. 2006; 48:19–24.

73. Jeong MH, Chung JW, Lee SJ, et al. Comparison of rifabutin- and levofloxacin-based third-line rescue therapies for Helicobacter pylori. Korean J Gastroenterol. 2012; 59:401–406.

74. Song MJ, Park DI, Park JH, et al. The effect of probiotics and mucoprotective agents on PPI-based triple therapy for eradication of Helicobacter pylori. Helicobacter. 2010; 15:206–213.

75. Szajewska H, Horvath A, Piwowarczyk A. Meta-analysis: the effects of Saccharomyces boulardii supplementation on Helicobacter pylori eradication rates and side effects during treatment. Aliment Pharmacol Ther. 2010; 32:1069–1079.

76. Wang ZH, Gao QY, Fang JY. Meta-analysis of the efficacy and safety of Lactobacillus-containing and Bifidobacterium-containing probiotic compound preparation in Helicobacter pylori eradication therapy. J Clin Gastroenterol. 2013; 47:25–32.

77. Nseir W, Diab H, Mahamid M, et al. Randomised clinical trial: sim-vastatin as adjuvant therapy improves significantly the Helicobacter pylori eradication rate–a placebo-controlled study. Aliment Pharmacol Ther. 2012; 36:231–238.

78. Leodolter A, Kulig M, Brasch H, Meyer-Sabellek W, Willich SN, Malfertheiner P. A metaanalysis comparing eradication, healing and relapse rates in patients with Helicobacter pylori-associated gastric or duodenal ulcer. Aliment Pharmacol Ther. 2001; 15:1949–1958.

79. Chan FKL, Ching J, Suen BY, Tse YK, Wu JC, Sung JJ. Effect of H. pylori eradication on the long-term incidence of recurrent ulcer bleeding in high-risk aspirin users: a 10-year prospective cohort study. Gastroenterology. 2011; 140:S173–S174.

80. Chan FK, Chung SC, Suen BY, et al. Preventing recurrent upper gastrointestinal bleeding in patients with Helicobacter pylori infection who are taking low-dose aspirin or naproxen. N Engl J Med. 2001; 344:967–973.

81. Lai KC, Lam SK, Chu KM, et al. Lansoprazole for the prevention of recurrences of ulcer complications from long-term low-dose aspirin use. N Engl J Med. 2002; 346:2033–2038.