Helicobacter pylori: Evidence-based review with a focus on immigrant populations

Journal of General Internal Medicine

Volumn 29, Issue 3, 2014, Pages 520-528

  Siao, Derrick ^a   Somsouk, Ma ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

dyspepsia; gastric adenocarcinoma; Helicobacter pylori; immigrant; peptic ulcer

Indexed keywords

BACTERIAL CLEARANCE; CANCER GROWTH; COST EFFECTIVENESS ANALYSIS; DYSPEPSIA; EVIDENCE BASED PRACTICE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; IMMIGRANT; PEPTIC ULCER; PRIMARY PREVENTION; RECURRENT DISEASE; REVIEW; STOMACH ADENOCARCINOMA; UNITED STATES;

EMIGRANTS AND IMMIGRANTS; EVIDENCE-BASED MEDICINE; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; PEPTIC ULCER; POPULATION SURVEILLANCE; STOMACH NEOPLASMS; UNITED STATES;

EID: 84896834208     PISSN: 08848734     EISSN: 15251497     Source Type: Journal    
DOI: 10.1007/s11606-013-2630-y     Document Type: Review

References (90)

1. Marshall BJ, Warren JR. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet. 1984;1(8390):1311-5.
2. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345(11):784-9. doi: 10.1056/NEJMoa001999.
3. Watanabe T, Tada M, Nagai H, Sasaki S, Nakao M. Helicobacter pylori infection induces gastric cancer in mongolian gerbils. Gastroenterology. 1998;115(3):642-8.
4. Wotherspoon AC, Diss TC, Pan LX, Schmid C, Kerr-Muir MG, Lea SH, et al. Primary low-grade B-cell lymphoma of the conjunctiva: a mucosa-associated lymphoid tissue type lymphoma. Histopathology. 1993;23(5):417-24.
5. DuBois S, Kearney DJ. Iron-deficiency anemia and Helicobacter pylori infection: a review of the evidence. Am J Gastroenterol. 2005;100(2):453-9. doi: 10.1111/j.1572-0241.2005.30252.x.
6. Emilia G, Luppi M, Zucchini P, Morselli M, Potenza L, Forghieri F, et al. Helicobacter pylori infection and chronic immune thrombocytopenic purpura: long-term results of bacterium eradication and association with bacterium virulence profiles. Blood. 2007;110(12):3833-41. doi: 10.1182/blood-2006-12- 063222.
7. Raghunath A, Hungin AP, Wooff D, Childs S. Prevalence of Helicobacter pylori in patients with gastro-oesophageal reflux disease: systematic review. BMJ. 2003;326(7392):737. doi: 10.1136/bmj.326.7392.737.
8. Moayyedi P, Deeks J, Talley NJ, Delaney B, Forman D. An update of the Cochrane systematic review of Helicobacter pylori eradication therapy in nonulcer dyspepsia: resolving the discrepancy between systematic reviews. Am J Gastroenterol. 2003;98(12):2621-6. doi: 10.1111/j.1572-0241.2003.08724.x.
9. Pounder RE, Ng D. The prevalence of Helicobacter pylori infection in different countries. Aliment Pharmacol Ther. 1995;9(Suppl 2):33-9.
10. Everhart JE. Recent developments in the epidemiology of Helicobacter pylori. Gastroenterol Clin N Am. 2000;29(3):559-78.
11. Grad YH, Lipsitch M, Aiello AE. Secular trends in Helicobacter pylori seroprevalence in adults in the United States: evidence for sustained race/ethnic disparities. Am J Epidemiol. 2012;175(1):54-9. doi: 10.1093/aje/kwr288.
12. Yeh JM, Hur C, Schrag D, Kuntz KM, Ezzati M, Stout N, et al. Contribution of H. pylori and smoking trends to US incidence of intestinal-type noncardia gastric adenocarcinoma: a microsimulation model. PLoS Med. 2013;10(5):e1001451.
13. Fock KM, Ang TL. Epidemiology of Helicobacter pylori infection and gastric cancer in Asia. J Gastroenterol Hepatol. 2010;25(3):479-86. doi: 10.1111/j.1440-1746.2009.06188.x.
14. Tsai CJ, Perry S, Sanchez L, Parsonnet J. Helicobacter pylori infection in different generations of Hispanics in the San Francisco Bay Area. Am J Epidemiol. 2005;162(4):351-7. doi: 10.1093/aje/kwi207.
15. Talley NJ.American Gastroenterological Association medical position statement: evaluation of dyspepsia. Gastroenterology. 2005;129(5):1753-5. doi: 10.1053/j.gastro.2005.09.019.
16. Hansen JM, Bytzer P.Value of the unaided clinical diagnosis in dyspeptic patients in primary care. Am J Gastroenterol. 2001;96(5):1417-21.
17. Hammer J, Eslick GD, Howell SC, Altiparmak E, Talley NJ. Diagnostic yield of alarm features in irritable bowel syndrome and functional dyspepsia. Gut. 2004;53(5):666-72.
18. Heikkinen M, Pikkarainen P, Takala J, Rasanen H, Julkunen R. Etiology of dyspepsia: four hundred unselected consecutive patients in general practice. Scand J Gastroenterol. 1995;30(6):519-23.
19. Chiba N, Van Zanten SJ, Sinclair P, Ferguson RA, Escobedo S, Grace E. Treating Helicobacter pylori infection in primary care patients with uninvestigated dyspepsia: the Canadian adult dyspepsia empiric treatment-Helicobacter pylori positive (CADET-Hp) randomised controlled trial. BMJ (Clin Res ed). 2002;324(7344):1012-6.
20. Huang JQ, Sridhar S, Hunt RH. Role of Helicobacter pylori infection and non-steroidal anti-inflammatory drugs in peptic-ulcer disease: a meta-analysis. Lancet. 2002;359(9300):14-22. doi: 10.1016/S0140-6736(02)07273-2.
21. Leodolter A, Kulig M, Brasch H, Meyer-Sabellek W, Willich SN, Malfertheiner P. A meta-analysis comparing eradication, healing and relapse rates in patients with Helicobacter pylori-associated gastric or duodenal ulcer. Aliment Pharmacol Ther. 2001;15(12):1949-58.
22. Malfertheiner P, Megraud F, O'Morain CA, Atherton J, Axon AT, Bazzoli F, et al. Management of Helicobacter pylori infection - the Maastricht IV/Florence Consensus Report. Gut. 2012;61(5):646-64. doi: 10.1136/gutjnl-2012-302084.
23. Chan FK, Ching JY, Suen BY, Tse YK, Wu JC, Sung JJ. Effects of Helicobacter pylori infection on long-term risk of peptic ulcer bleeding in low-dose aspirin users. Gastroenterology. 2013;144(3):528-35. doi: 10.1053/j.gastro.2012.12.038.
24. Loy CT, Irwig LM, Katelaris PH, Talley NJ. Do commercial serological kits for Helicobacter pylori infection differ in accuracy? A meta-analysis. Am J Gastroenterol. 1996;91(6):1138-44.
25. Nurgalieva ZZ, Graham DY. Pearls and pitfalls of assessing Helicobacter pylori status. Dig Liver Dis. 2003;35(6):375-7.
26. Chey WD. Accurate diagnosis of Helicobacter pylori. 14C-urea breath test. Gastroenterol Clin N Am. 2000;29(4):895-902.
27. Peura DA, Pambianco DJ, Dye KR, Lind C, Frierson HF, Hoffman SR, et al. Microdose 14C-urea breath test offers diagnosis of Helicobacter pylori in 10 minutes. Am J Gastroenterol. 1996;91(2):233-8.
28. Chey WD, Wong BC. Practice parameters committee of the American College of G. American College of Gastroenterology guideline on the management of Helicobacter pylori infection. Am J Gastroenterol. 2007;102(8):1808-25. doi: 10.1111/j.1572-0241.2007.01393.x.
29. Chey WD, Woods M, Scheiman JM, Nostrant TT, DelValle J. Lansoprazole and ranitidine affect the accuracy of the 14C-urea breath test by a pH-dependent mechanism. Am J Gastroenterol. 1997;92(3):446-50.
30. Stermer E, Levy N, Tabak M, Neeman I. Lanzoprazole and ranitidine affect the accuracy of the 14C-urea breath test by a pH-dependent mechanism. Am J Gastroenterol. 1997;92(9):1575-6.
31. Gisbert JP, Pajares JM. Stool antigen test for the diagnosis of Helicobacter pylori infection: a systematic review. Helicobacter. 2004;9(4):347-68. doi: 10.1111/j.1083-4389.2004.00235.x.
32. Bravo LE, Realpe JL, Campo C, Mera R, Correa P. Effects of acid suppression and bismuth medications on the performance of diagnostic tests for Helicobacter pylori infection. Am J Gastroenterol. 1999;94(9):2380-3. doi: 10.1111/j.1572-0241.1999.01361.x.
33. Hansen S, Melby KK, Aase S, Jellum E, Vollset SE. Helicobacter pylori infection and risk of cardia cancer and non-cardia gastric cancer. A nested case-control study. Scand J Gastroenterol. 1999;34(4):353-60.
34. Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, et al. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med. 1991;325(16):1127-31. doi: 10.1056/NEJM199110173251603.
35. International Agency for Research on Cancer. Schistosomes, liver flukes and Helicobacter pylori. IARC working group on the evaluation of carcinogenic risks to humans. Lyon, 7-14 June 1994. IARC monographs on the evaluation of carcinogenic risks to humans/World Health Organization, International Agency for Research on Cancer. 1994;61:1-241.
36. Brenner H, Arndt V, Stegmaier C, Ziegler H, Rothenbacher D. Is Helicobacter pylori infection a necessary condition for noncardia gastric cancer? Am J Epidemiol. 2004;159(3):252-8.
37. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process-First American cancer society award lecture on cancer epidemiology and prevention. Cancer Res. 1992;52(24):6735-40.
38. Kuipers EJ, Uyterlinde AM, Pena AS, Roosendaal R, Pals G, Nelis GF, et al. Long-term sequelae of Helicobacter pylori gastritis. Lancet. 1995;345(8964):1525-8.
39. Yakirevich E, Resnick MB. Pathology of gastric cancer and its precursor lesions. Gastroenterol Clin North Am. 2013;42(2):261-84. doi: 10.1016/j.gtc.2013.01.004.
40. Fox JG, Wang TC. Inflammation, atrophy, and gastric cancer. J Clin Investigat. 2007;117(1):60-9. doi: 10.1172/JCI30111.
41. El-Omar EM, Carrington M, Chow WH, McColl KE, Bream JH, Young HA, et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature. 2000;404(6776):398-402. doi: 10.1038/35006081.
42. El-Omar EM, Oien K, Murray LS, El-Nujumi A, Wirz A, Gillen D, et al. Increased prevalence of precancerous changes in relatives of gastric cancer patients: critical role of H. pylori. Gastroenterology. 2000;118(1):22-30.
43. Joossens JV, Hill MJ, Elliott P, Stamler R, Lesaffre E, Dyer A, et al. Dietary salt, nitrate and stomach cancer mortality in 24 countries. European Cancer Prevention (ECP) and the INTERSALT Cooperative Research Group. Int J Epidemiol. 1996;25(3):494-504.
44. Chen MJ, Wu DC, Ko YC, Chiou YY. Personal history and family history as a predictor of gastric cardiac adenocarcinoma risk: a case-control study in Taiwan. Am J Gastroenterol. 2004;99(7):1250-7. doi: 10.1111/j.1572-0241.2004. 30872.x.
45. Lau M, Le A, El-Serag HB. Noncardia gastric adenocarcinoma remains an important and deadly cancer in the United States: secular trends in incidence and survival. Am J Gastroenterol. 2006;101(11):2485-92. doi: 10.1111/j.1572-0241.2006.00778.x.
46. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. International journal of cancer. J Int du Cancer. 2010;127(12):2893-917. doi: 10.1002/ijc.25516.
47. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55(2):74-108.
48. Talley NJ, Fock KM, Moayyedi P. Gastric Cancer Consensus conference recommends Helicobacter pylori screening and treatment in asymptomatic persons from high-risk populations to prevent gastric cancer. Am J Gastroenterol. 2008;103(3):510-4. doi: 10.1111/j.1572-0241.2008.01819.x.
49. Howe HL, Wu X, Ries LA, Cokkinides V, Ahmed F, Jemal A, et al. Annual report to the nation on the status of cancer, 1975-2003, featuring cancer among U.S. Hispanic/Latino populations. Cancer. 2006;107(8):1711-42.
50. Hirota WK, Zuckerman MJ, Adler DG, Davila RE, Egan J, Leighton JA, et al. ASGE guideline: the role of endoscopy in the surveillance of premalignant conditions of the upper GI tract. Gastrointest Endosc. 2006;63(4):570-80. doi: 10.1016/j.gie.2006.02.004.
51. Uemura N, Mukai T, Okamoto S, Yamaguchi S, Mashiba H, Taniyama K, et al. Effect of Helicobacter pylori eradication on subsequent development of cancer after endoscopic resection of early gastric cancer. Cancer Epidemiol Biomark Prev. 1997;6(8):639-42.
52. 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(9636):392-7. doi: 10.1016/S0140-6736(08)61159-9.
53. Kato M, Asaka M. Recent knowledge of the relationship between Helicobacter pylori and gastric cancer and recent progress of gastroendoscopic diagnosis and treatment for gastric cancer. Jpn J Clin Oncol. 2010;40(9):828-37. doi: 10.1093/jjco/hyq119.
54. Rokkas T, Sechopoulos P, Robotis I, Margantinis G, Pistiolas D. Cumulative H. pylori eradication rates in clinical practice by adopting first and second-line regimens proposed by the Maastricht III consensus and a third-line empirical regimen. Am J Gastroenterol. 2009;104(1):21-5. doi: 10.1038/ajg.2008.87.
55. Zhou L, Sung JJ, Lin S, Jin Z, Ding S, Huang X, et al. A five-year follow-up study on the pathological changes of gastric mucosa after H. pylori eradication. Chin Med J. 2003;116(1):11-4.
56. Fuccio L, Zagari RM, Eusebi LH, Laterza L, Cennamo V, Ceroni L, et al. Meta-analysis: can Helicobacter pylori eradication treatment reduce the risk for gastric cancer? Ann Intern Med. 2009;151(2):121-8.
57. Fock KM, Katelaris P, Sugano K, Ang TL, Hunt R, Talley NJ, et al. Second Asia-Pacific Consensus Guidelines for Helicobacter pylori infection. J Gastroenterol Hepatol. 2009;24(10):1587-600. doi: 10.1111/j.1440-1746.2009. 05982.x.
58. Fock KM, Talley N, Moayyedi P, Hunt R, Azuma T, Sugano K, et al. Asia-Pacific consensus guidelines on gastric cancer prevention. J Gastroenterol Hepatol. 2008;23(3):351-65. doi: 10.1111/j.1440-1746.2008.05314.x.
59. Malfertheiner P, Sipponen P, Naumann M, Moayyedi P, Megraud F, Xiao SD, et al. Helicobacter pylori eradication has the potential to prevent gastric cancer: a state-of-the-art critique. Am J Gastroenterol. 2005;100(9):2100-15. doi: 10.1111/j.1572-0241.2005.41688.x.
60. Graham DY, Lu H, Yamaoka Y. A report card to grade Helicobacter pylori therapy. Helicobacter. 2007;12(4):275-8. doi: 10.1111/j.1523-5378.2007.00518.x.
61. Katelaris PH, Forbes GM, Talley NJ, Crotty B. A randomized comparison of quadruple and triple therapies for Helicobacter pylori eradication: The QUADRATE Study. Gastroenterology. 2002;123(6):1763-9. doi: 10.1053/gast.2002.37051.
62. Luther J, Higgins PD, Schoenfeld PS, Moayyedi P, Vakil N, Chey WD. Empiric quadruple vs. triple therapy for primary treatment of Helicobacter pylori infection: Systematic review and meta-analysis of efficacy and tolerability. Am J Gastroenterol. 2010;105(1):65-73. doi: 10.1038/ajg.2009.508.
63. Gene E, Calvet X, Azagra R, Gisbert JP. Triple vs quadruple therapy for treating Helicobacter pylori infection: an updated meta-analysis. Aliment Pharmacol Ther. 2003;18(5):543-4.
64. Osato MS, Reddy R, Reddy SG, Penland RL, Malaty HM, Graham DY. Pattern of primary resistance of Helicobacter pylori to metronidazole or clarithromycin in the United States. Arch Intern Med. 2001;161(9):1217-20.
65. McMahon BJ, Hennessy TW, Bensler JM, Bruden DL, Parkinson AJ, Morris JM, et al. The relationship among previous antimicrobial use, antimicrobial resistance, and treatment outcomes for Helicobacter pylori infections. Ann Intern Med. 2003;139(6):463-9.
66. Fischbach LA, Goodman KJ, Feldman M, Aragaki C. Sources of variation of Helicobacter pylori treatment success in adults worldwide: a meta-analysis. Int J Epidemiol. 2002;31(1):128-39.
67. Graham DY, Fischbach L. Helicobacter pylori treatment in the era of increasing antibiotic resistance. Gut. 2010;59(8):1143-53. doi: 10.1136/gut.2009.192757.
68. Vaira D, Zullo A, Vakil N, Gatta L, Ricci C, Perna F, et al. Sequential therapy versus standard triple-drug therapy for Helicobacter pylori eradication: a randomized trial. Ann Intern Med. 2007;146(8):556-63.
69. Liou JM, Chen CC, Chen MJ, Chen CC, Chang CY, Fang YJ, et al. Sequential versus triple therapy for the first-line treatment of Helicobacter pylori: a multicentre, open-label, randomised trial. Lancet. 2013;381(9862):205-13. doi: 10.1016/S0140-6736(12)61579-7.
70. Hojo M, Miwa H, Nagahara A, Sato N. Pooled analysis on the efficacy of the second-line treatment regimens for Helicobacter pylori infection. Scand J Gastroenterol. 2001;36(7):690-700.
71. Gisbert JP, Gisbert JL, Marcos S, Jimenez-Alonso I, Moreno-Otero R, Pajares JM. Empirical rescue therapy after Helicobacter pylori treatment failure: a 10-year single-centre study of 500 patients. Aliment Pharmacol Ther. 2008;27(4):346-54. doi: 10.1111/j.1365-2036.2007.03573.x.
72. Basu PP, Rayapudi K, Pacana T, Shah NJ, Krishnaswamy N, Flynn M. A randomized study comparing levofloxacin, omeprazole, nitazoxanide, and doxycycline versus triple therapy for the eradication of Helicobacter pylori. Am J Gastroenterol. 2011;106(11):1970-5.
73. Romano M, Cuomo A, Gravina AG, Miranda A, Iovene MR, Tiso A, et al. Empirical levofloxacin-containing versus clarithromycin-containing sequential therapy for Helicobacter pylori eradication: a randomised trial. Gut. 2010;59(11):1465-70. doi: 10.1136/gut.2010.215350.
74. Saad RJ, Schoenfeld P, Kim HM, Chey WD. Levofloxacin-based triple therapy versus bismuth-based quadruple therapy for persistent Helicobacter pylori infection: a meta-analysis. Am J Gastroenterol. 2006;101(3):488-96. doi: 10.1111/j.1572-0241.1998.455-t.x.
75. Tay CY, Windsor HM, Thirriot F, Lu W, Conway C, Perkins TT, et al. Helicobacter pylori eradication in Western Australia using novel quadruple therapy combinations. Aliment Pharmacol Ther. 2012;36(11-12):1076-83. doi: 10.1111/apt.12089.
76. Yun SP, Seon HG, Ok CS, Yoo KH, Kang MK, Kim WH, et al. Rifaximin plus levofloxacin-based rescue regimen for the eradication of Helicobacter pylori. Gut Liver. 2012;6(4):452-6. doi: 10.5009/gnl.2012.6.4.452.
77. Hopkins RJ, Girardi LS, Turney EA. Relationship between Helicobacter pylori eradication and reduced duodenal and gastric ulcer recurrence: a review. Gastroenterology. 1996;110(4):1244-52.
78. Lee M, Kemp JA, Canning A, Egan C, Tataronis G, Farraye FA. A randomized controlled trial of an enhanced patient compliance program for Helicobacter pylori therapy. Arch Intern Med. 1999;159(19):2312-6.
79. Graham DY, Lew GM, Malaty HM, Evans DG, Evans DJ Jr, Klein PD, et al. Factors influencing the eradication of Helicobacter pylori with triple therapy. Gastroenterology. 1992;102(2):493-6.
80. Morgan DR, Torres J, Sexton R, Herrero R, Salazar-Martinez E, Greenberg ER, et al. Risk of recurrent Helicobacter pylori infection 1 year after initial eradication therapy in 7 Latin American communities. JAMA. 2013;309(6):578-86. doi: 10.1001/jama.2013.311.
81. Sonnenberg A, Everhart JE. Health impact of peptic ulcer in the United States. Am J Gastroenterol. 1997;92(4):614-20.
82. Sonnenberg A, Schwartz JS, Cutler AF, Vakil N, Bloom BS. Cost savings in duodenal ulcer therapy through Helicobacter pylori eradication compared with conventional therapies: results of a randomized, double-blind, multicenter trial. Gastrointestinal Utilization Trial Study Group. Arch Intern Med. 1998;158(8):852-60.
83. Mapel D, Roberts M, Overhiser A, Mason A. The epidemiology, diagnosis, and cost of dyspepsia and Helicobacter pylori gastritis: a case-control analysis in the Southwestern United States. Helicobacter. 2013;18(1):54-65. doi: 10.1111/j.1523-5378.2012.00988.x.
84. Mason J, Axon AT, Forman D, Duffett S, Drummond M, Crocombe W, et al. The cost-effectiveness of population Helicobacter pylori screening and treatment: a Markov model using economic data from a randomized controlled trial. Aliment Pharmacol Ther. 2002;16(3):559-68.
85. Ford AC, Forman D, Bailey AG, Axon AT, Moayyedi P. A community screening program for Helicobacter pylori saves money: 10-year follow-up of a randomized controlled trial. Gastroenterology. 2005;129(6):1910-7. doi: 10.1053/j.gastro.2005.09.016.
86. Everhart JE, Ruhl CE. Burden of digestive diseases in the United States part I: overall and upper gastrointestinal diseases. Gastroenterology. 2009;136(2):376-86. doi: 10.1053/j.gastro.2008.12.015.
87. Areia M, Carvalho R, Cadime AT, Rocha Goncalves F, Dinis-Ribeiro M. Screening for gastric cancer and surveillance of premalignant lesions: a systematic review of cost-effectiveness studies. Helicobacter. 2013. doi: 10.1111/hel.12050.
88. Leivo T, Salomaa A, Kosunen TU, Tuominen R, Farkkila M, Linna M, et al. Cost-benefit analysis of Helicobacter pylori screening. Health policy. 2004;70(1):85-96. doi: 10.1016/j.healthpol.2004.02.004.
89. Fischbach L, Evans EL. Meta-analysis: the effect of antibiotic resistance status on the efficacy of triple and quadruple first-line therapies for Helicobacter pylori. Aliment Pharmacol Ther. 2007;26(3):343-57. doi: 10.1111/j.1365-2036.2007.03386.x.
90. Zullo A, De Francesco V, Hassan C, Morini S, Vaira D. The sequential therapy regimen for Helicobacter pylori eradication: a pooled-data analysis. Gut. 2007;56(10):1353-7. doi: 10.1136/gut.2007.125658.