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Helicobacter pylori infection and gastric cardia cancer: systematic review and meta-analysis

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Abstract

Objective

Helicobacter pylori infection is the most important risk factor for gastric cancer, but no association with cardia cancer has been recognized. However, a heterogeneous distribution of etiologically distinct types of cardia cancer may contribute to explain conflicting findings between studies in high- and low-risk settings. We aimed to quantify the association between H. pylori infection and gastric cardia cancer through meta-analysis, and to provide an explanation for the expected heterogeneity of results.

Methods

We systematically reviewed published studies addressing the association between H. pylori infection and gastric cardia cancer (up to June 2009), and extracted relative risk (RR) estimates for the association with cardia and non-cardia cancers. Summary RR estimates and 95% confidence intervals (95% CI) were computed using random-effects models. Subgroup analyses were conducted, namely according to gastric cancer risk settings.

Results

Thirty-four articles were considered for meta-analysis. For cardia cancer, summary RR was 1.08 (95% CI 0.83–1.40; I 2 = 52.8%), higher in high-risk (RR = 1.98; 95% CI 1.38–2.83; I 2 = 18.4%) than in low-risk settings (RR = 0.78; 95% CI 0.63–0.97; I 2 = 11.6%). For non-cardia cancer, RR estimates were similar in high- (RR = 3.02; 95% CI 1.92–4.74; I 2 = 90.7%) and low-risk settings (RR = 2.56; 95% CI 1.99–3.29; I 2 = 46.6%). These observations were consistent across different inclusion criteria and when accounting for the virulence of the infecting strains.

Conclusions

In high-risk settings, a positive association between H. pylori infection and gastric cancer was observed both for cardia and non-cardia cancers. The results support the hypothesis of a heterogeneous distribution of etiologically distinct types of cardia cancer.

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References

  1. Parkin DM, Whelan SL, Ferlay J, Teppo L, Thomas BD (2002) Cancer incidence in five continents. IARC Sci Publ No. 155. IARC, Lyon

    Google Scholar 

  2. Armstrong RW, Borman B (1996) Trends in incidence rates of adenocarcinoma of the oesophagus and gastric cardia in New Zealand, 1978–1992. Int J Epidemiol 25:941–947

    Article  CAS  PubMed  Google Scholar 

  3. Bertuccio P, Chatenoud L, Levi F et al (2009) Recent patterns in gastric cancer: a global overview. Int J Cancer 125:666–673

    Article  CAS  PubMed  Google Scholar 

  4. Hansen S, Wiig JN, Giercksky KE, Tretli S (1997) Esophageal and gastric carcinoma in Norway 1958–1992: incidence time trend variability according to morphological subtypes and organ subsites. Int J Cancer 71:340–344

    Article  CAS  PubMed  Google Scholar 

  5. Pera M, Cameron AJ, Trastek VF, Carpenter HA, Zinsmeister AR (1993) Increasing incidence of adenocarcinoma of the esophagus and esophagogastric junction. Gastroenterology 104:510–513

    CAS  PubMed  Google Scholar 

  6. Moller H (1992) Incidence of cancer of oesophagus, cardia and stomach in Denmark. Eur J Cancer Prev 1:159–164

    Article  CAS  PubMed  Google Scholar 

  7. Harrison SL, Goldacre MJ, Seagroatt V (1992) Trends in registered incidence of oesophageal and stomach cancer in the Oxford region, 1974–88. Eur J Cancer Prev 1:271–274

    Article  CAS  PubMed  Google Scholar 

  8. Levi F, La Vecchia C, Te VC (1990) Descriptive epidemiology of adenocarcinomas of the cardia and distal stomach in the Swiss Canton of Vaud. Tumori 76:167–171

    CAS  PubMed  Google Scholar 

  9. Thomas RJ, Lade S, Giles GG, Thursfield V (1996) Incidence trends in oesophageal and proximal gastric carcinoma in Victoria. Aust N Z J Surg 66:271–275

    Article  CAS  PubMed  Google Scholar 

  10. Correa P, Haenszel W, Cuello C, Tannenbaum S, Archer M (1975) A model for gastric cancer epidemiology. Lancet 2:58–60

    Article  CAS  PubMed  Google Scholar 

  11. Popiela T, Kulig J, Kolodziejczyk P, Sierzega M (2002) Changing patterns of gastric carcinoma over the past two decades in a single institution: clinicopathological findings in 1557 patients. Scand J Gastroenterol 37:561–567

    Article  CAS  PubMed  Google Scholar 

  12. Lee JY, Kim HY, Kim KH et al (2003) No changing trends in incidence of gastric cardia cancer in Korea. J Korean Med Sci 18:53–57

    PubMed  Google Scholar 

  13. Blot WJ, Devesa SS, Kneller RW, Fraumeni JF Jr (1991) Rising incidence of adenocarcinoma of the esophagus and gastric cardia. JAMA 265:1287–1289

    Article  CAS  PubMed  Google Scholar 

  14. Bouvier AM, Esteve J, Mitry E, Clinard F, Bonithon-Kopp C, Faivre J (2002) Trends in gastric cancer incidence in a well-defined French population by time period and birth cohort. Eur J Cancer Prev 11:221–227

    Article  PubMed  Google Scholar 

  15. Crane SJ, Richard Locke G III, Harmsen WS et al (2007) The changing incidence of oesophageal and gastric adenocarcinoma by anatomic sub-site. Aliment Pharmacol Ther 25:447–453

    Article  CAS  PubMed  Google Scholar 

  16. Huang JQ, Hunt RH (2003) The evolving epidemiology of Helicobacter pylori infection and gastric cancer. Can J Gastroenterol 17(Suppl B):18B–20B

    PubMed  Google Scholar 

  17. Eslick GD, Lim LL, Byles JE, Xia HH, Talley NJ (1999) Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis. Am J Gastroenterol 94:2373–2379

    Article  CAS  PubMed  Google Scholar 

  18. Huang JQ, Sridhar S, Chen Y, Hunt RH (1998) Meta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer. Gastroenterology 114:1169–1179

    Article  CAS  PubMed  Google Scholar 

  19. Webb PM, Law M, Varghese C, Forman D, Yuan JM, Yu M, Ross R, Limberg PJ, Mark SD, Taylor PR, Dawsey SM, Qiao YL, Aromaa A, Knekt P, Kosunen TU, Heinonen OP, Virtamo J, Tulinius H, Watanabe Y, Ozasa K, Kurata JH, Hansen S, Melby KK, Aase S, Jellum E, Vollset SE, Siman JH, Forsgren A, Berglund G, Floren CH, Lin JT, Chen CJ, Wald NJ, Parsonnet J, Friedman GD, Blaser MJ, Nomura A, Stemmermann GN (2001) Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut 49:347–353

    Article  Google Scholar 

  20. Huang JQ, Zheng GF, Sumanac K, Irvine EJ, Hunt RH (2003) Meta-analysis of the relationship between cagA seropositivity and gastric cancer. Gastroenterology 125:1636–1644

    Article  PubMed  Google Scholar 

  21. Dawsey SM, Mark SD, Taylor PR, Limburg PJ (2002) Gastric cancer and H. pylori. Gut 51:457–458

    Article  CAS  PubMed  Google Scholar 

  22. Limburg P, Qiao Y, Mark S et al (2001) Helicobacter pylori seropositivity and subsite-specific gastric cancer risks in Linxian, China. J Natl Cancer Inst 93:226–233

    Article  CAS  PubMed  Google Scholar 

  23. Chow WH, Blaser MJ, Blot WJ et al (1998) An inverse relation between cagA + strains of Helicobacter pylori infection and risk of esophageal and gastric cardia adenocarcinoma. Cancer Res 58:588–590

    CAS  PubMed  Google Scholar 

  24. Brenner H, Arndt V, Stegmaier C, Ziegler H, Rothenbacher D (2004) Is Helicobacter pylori infection a necessary condition for noncardia gastric cancer? Am J Epidemiol 159:252–258

    Article  PubMed  Google Scholar 

  25. Nomura AM, Kolonel LN, Miki K et al (2005) Helicobacter pylori, pepsinogen, and gastric adenocarcinoma in Hawaii. J Infect Dis 191:2075–2081

    Article  CAS  PubMed  Google Scholar 

  26. Kamangar F, Dawsey SM, Blaser MJ et al (2006) Opposing risks of gastric cardia and noncardia gastric adenocarcinomas associated with Helicobacter pylori seropositivity. J Natl Cancer Inst 98:1445–1452

    Article  PubMed  Google Scholar 

  27. Talley NJ, Zinsmeister AR, Weaver A et al (1991) Gastric adenocarcinoma and Helicobacter pylori infection. J Natl Cancer Inst 83:1734–1739

    Article  CAS  PubMed  Google Scholar 

  28. Shibata T, Imoto I, Ohuchi Y et al (1996) Helicobacter pylori infection in patients with gastric carcinoma in biopsy and surgical resection specimens. Cancer 77:1044–1049

    Article  CAS  PubMed  Google Scholar 

  29. Fukuda H, Saito D, Hayashi S et al (1995) Helicobacter pylori infection, serum pepsinogen level and gastric cancer: a case–control study in Japan. Jpn J Cancer Res 86:64–71

    CAS  PubMed  Google Scholar 

  30. Kim HY, Cho BD, Chang WK et al (1997) Helicobacter pylori infection and the risk of gastric cancer among the Korean population. J Gastroenterol Hepatol 12:100–103

    Article  CAS  PubMed  Google Scholar 

  31. Kamangar F, Qiao YL, Blaser MJ et al (2007) Helicobacter pylori and oesophageal and gastric cancers in a prospective study in China. Br J Cancer 96:172–176

    Article  CAS  PubMed  Google Scholar 

  32. Lunet N (2006) Gastric cancer frequency and trends. Arq Med 20:79–85

    Google Scholar 

  33. Wu AH, Crabtree JE, Bernstein L et al (2003) Role of Helicobacter pylori CagA + strains and risk of adenocarcinoma of the stomach and esophagus. Int J Cancer 103:815–821

    Article  CAS  PubMed  Google Scholar 

  34. Shen J, Wang RT, Wang LW, Xu YC, Wang XR (2004) A novel genetic polymorphism of inducible nitric oxide synthase is associated with an increased risk of gastric cancer. World J Gastroenterol 10:3278–3283

    CAS  PubMed  Google Scholar 

  35. Kokkola A, Louhimo J, Puolakkainen P, Alfthan H, Haglund C, Rautelin H (2005) Helicobacter pylori infection and low serum pepsinogen I level as risk factors for gastric carcinoma. World J Gastroenterol 11:1032–1036

    CAS  PubMed  Google Scholar 

  36. Held M, Engstrand L, Hansson LE, Bergstrom R, Wadstrom T, Nyren O (2004) Is the association between Helicobacter pylori and gastric cancer confined to CagA-positive strains? Helicobacter 9:271–277

    Article  PubMed  Google Scholar 

  37. Queiroz DM, Mendes EN, Rocha GA et al (1998) CagA-positive Helicobacter pylori and risk for developing gastric carcinoma in Brazil. Int J Cancer 78:135–139

    Article  CAS  PubMed  Google Scholar 

  38. Yamaoka Y, Kodama T, Kashima K, Graham DY (1999) Antibody against Helicobacter pylori CagA and VacA and the risk for gastric cancer. J Clin Pathol 52:215–218

    Article  CAS  PubMed  Google Scholar 

  39. Mitchell H, English DR, Elliott F et al (2008) Immunoblotting using multiple antigens is essential to demonstrate the true risk of Helicobacter pylori infection for gastric cancer. Aliment Pharmacol Ther 28:903–910

    CAS  PubMed  Google Scholar 

  40. Lin JT, Wang JT, Wang TH, Wu MS, Lee TK, Chen CJ (1993) Helicobacter pylori infection in a randomly selected population, healthy volunteers, and patients with gastric ulcer and gastric adenocarcinoma. A seroprevalence study in Taiwan. Scand J Gastroenterol 28:1067–1072

    Article  CAS  PubMed  Google Scholar 

  41. Lee BM, Jang JJ, Kim JS et al (1998) Association of Helicobacter pylori infection with gastric adenocarcinoma. Jpn J Cancer Res 89:597–603

    CAS  PubMed  Google Scholar 

  42. Kikuchi S, Crabtree JE, Forman D, Kurosawa M (1999) Association between infections with CagA-positive or -negative strains of Helicobacter pylori and risk for gastric cancer in young adults. Research Group on Prevention of Gastric Carcinoma Among Young Adults. Am J Gastroenterol 94:3455–3459

    Article  CAS  PubMed  Google Scholar 

  43. Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558

    Article  PubMed  Google Scholar 

  44. GLOBOCAN 2002 (2004) Cancer incidence, mortality and prevalence worlwide [database on the Internet]. IARC Press, Lyon

    Google Scholar 

  45. Society AC (2004) Hawaii cancer facts & figures 2003–2004

  46. Crew KD, Neugut AI (2006) Epidemiology of gastric cancer. World J Gastroenterol 12:354–362

    PubMed  Google Scholar 

  47. Curado MP, Edwards B, Shin HR, Storm H, Ferlay J, Heanue M, Boyle P (eds) (2007) Cancer incidence in five continents, vol IX. IARC Scientific Publications No. 160. IARC, Lyon

    Google Scholar 

  48. Parsonnet J, Friedman GD, Vandersteen DP et al (1991) Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 325:1127–1131

    Article  CAS  PubMed  Google Scholar 

  49. Lin JT, Wang JT, Wang TH, Wu MS, Chen CJ (1993) Helicobacter pylori infection in early and advanced gastric adenocarcinoma: a seroprevalence study in 143 Taiwanese patients. Hepatogastroenterology 40:596–599

    CAS  PubMed  Google Scholar 

  50. Hansson LE, Engstrand L, Nyren O et al (1993) Helicobacter pylori infection: independent risk indicator of gastric adenocarcinoma. Gastroenterology 105:1098–1103

    CAS  PubMed  Google Scholar 

  51. Kikuchi S, Wada O, Nakajima T et al (1995) Serum anti-Helicobacter pylori antibody and gastric carcinoma among young adults. Research Group on Prevention of Gastric Carcinoma among Young Adults. Cancer 75:2789–2793

    Article  CAS  PubMed  Google Scholar 

  52. Webb PM, Yu MC, Forman D et al (1996) An apparent lack of association between Helicobacter pylori infection and risk of gastric cancer in China. Int J Cancer 67:603–607

    Article  CAS  PubMed  Google Scholar 

  53. Siman JH, Forsgren A, Berglund G, Floren CH (1997) Association between Helicobacter pylori and gastric carcinoma in the city of Malmo, Sweden. A prospective study. Scand J Gastroenterol 32:1215–1221

    Article  CAS  PubMed  Google Scholar 

  54. Brenner H, Arndt V, Sturmer T, Stegmaier C, Ziegler H, Dhom G (2000) Individual and joint contribution of family history and Helicobacter pylori infection to the risk of gastric carcinoma. Cancer 88:274–279

    Article  CAS  PubMed  Google Scholar 

  55. Brenner H, Arndt V, Bode G, Stegmaier C, Ziegler H, Stumer T (2002) Risk of gastric cancer among smokers infected with Helicobacter pylori. Int J Cancer 98:446–449

    Article  CAS  PubMed  Google Scholar 

  56. Enroth H, Kraaz W, Rohan T, Nyren O, Engstrand L (2002) Does the method of Helicobacter pylori detection influence the association with gastric cancer risk? Scand J Gastroenterol 37:884–890

    Article  CAS  PubMed  Google Scholar 

  57. Gonzalez CA, Jakszyn P, Pera G et al (2006) Meat intake and risk of stomach and esophageal adenocarcinoma within the European Prospective Investigation into Cancer and Nutrition (EPIC). J Natl Cancer Inst 98:345–354

    Article  PubMed  Google Scholar 

  58. Gonzalez CA, Pera G, Agudo A et al (2006) Fruit and vegetable intake and the risk of stomach and oesophagus adenocarcinoma in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST). Int J Cancer 118:2559–2566

    Article  CAS  PubMed  Google Scholar 

  59. Hansen S, Vollset SE, Derakhshan MH et al (2007) Two distinct aetiologies of cardia cancer; evidence from premorbid serological markers of gastric atrophy and Helicobacter pylori status. Gut 56:918–925

    Article  CAS  PubMed  Google Scholar 

  60. Ren JS, Qiao YL (2008) Helicobacter pylori infection and gastric cardia cancer: a nested case–control study. Zhonghua Zhong Liu Za Zhi 30:428–431

    PubMed  Google Scholar 

  61. Estevens J, Fidalgo P, Tendeiro T et al (1993) Anti-Helicobacter pylori antibodies prevalence and gastric adenocarcinoma in Portugal: report of a case–control study. Eur J Cancer Prev 2:377–380

    Article  CAS  PubMed  Google Scholar 

  62. Blaser MJ, Perez-Perez GI, Kleanthous H et al (1995) Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 55:2111–2115

    CAS  PubMed  Google Scholar 

  63. Aromaa A, Kosunen TU, Knekt P et al (1996) Circulating anti-Helicobacter pylori immunoglobulin A antibodies and low serum pepsinogen I level are associated with increased risk of gastric cancer. Am J Epidemiol 144:142–149

    CAS  PubMed  Google Scholar 

  64. Martin-de-Argila C, Boixeda D, Redondo C et al (1997) Relation between histologic subtypes and location of gastric cancer and Helicobacter pylori. Scand J Gastroenterol 32:303–307

    Article  CAS  PubMed  Google Scholar 

  65. Erkisi M, Colakoglu S, Koksal F et al (1997) Relationship of Helicobacter pylori infection to several malignant and non-malignant gastrointestinal diseases. J Exp Clin Cancer Res 16:289–293

    CAS  PubMed  Google Scholar 

  66. Whiting JL, Hallissey MT, Fielding JW, Dunn J (1998) Screening for gastric cancer by Helicobacter pylori serology: a retrospective study. Br J Surg 85:408–411

    Article  CAS  PubMed  Google Scholar 

  67. Louw JA, Kidd MS, Kummer AF, Taylor K, Kotze U, Hanslo D (2001) The relationship between Helicobacter pylori infection, the virulence genotypes of the infecting strain and gastric cancer in the African setting. Helicobacter 6:268–273

    Article  CAS  PubMed  Google Scholar 

  68. Watabe H, Mitsushima T, Yamaji Y et al (2005) Predicting the development of gastric cancer from combining Helicobacter pylori antibodies and serum pepsinogen status: a prospective endoscopic cohort study. Gut 54:764–768

    Article  CAS  PubMed  Google Scholar 

  69. Suzuki G, Cullings H, Fujiwara S et al (2007) Low-positive antibody titer against Helicobacter pylori cytotoxin-associated gene A (CagA) may predict future gastric cancer better than simple seropositivity against H. pylori CagA or against H. pylori. Cancer Epidemiol Biomarkers Prev 16:1224–1228

    Article  CAS  PubMed  Google Scholar 

  70. Palli D, Masala G, Del Giudice G et al (2007) CagA + Helicobacter pylori infection and gastric cancer risk in the EPIC-EURGAST study. Int J Cancer 120:859–867

    Article  CAS  PubMed  Google Scholar 

  71. Knekt P, Teppo L, Aromaa A, Rissanen H, Kosunen TU (2006) Helicobacter pylori IgA and IgG antibodies, serum pepsinogen I and the risk of gastric cancer: changes in the risk with extended follow-up period. Int J Cancer 119:702–705

    Article  CAS  PubMed  Google Scholar 

  72. Ekstrom AM, Held M, Hansson LE, Engstrand L, Nyren O (2001) Helicobacter pylori in gastric cancer established by CagA immunoblot as a marker of past infection. Gastroenterology 121:784–791

    Article  CAS  PubMed  Google Scholar 

  73. Siman JH, Engstrand L, Berglund G, Forsgren A, Floren CH (2007) Helicobacter pylori and CagA seropositivity and its association with gastric and oesophageal carcinoma. Scand J Gastroenterol 42:933–940

    Article  CAS  PubMed  Google Scholar 

  74. Rudi J, Muller M, von Herbay A et al (1995) Lack of association of Helicobacter pylori seroprevalence and gastric cancer in a population with low gastric cancer incidence. Scand J Gastroenterol 30:958–963

    Article  CAS  PubMed  Google Scholar 

  75. Hansen S, Melby KK, Aase S, Jellum E, Vollset SE (1999) Helicobacter pylori infection and risk of cardia cancer and non-cardia gastric cancer. A nested case–control study. Scand J Gastroenterol 34:353–360

    Article  CAS  PubMed  Google Scholar 

  76. Ye W, Held M, Lagergren J et al (2004) Helicobacter pylori infection and gastric atrophy: risk of adenocarcinoma and squamous-cell carcinoma of the esophagus and adenocarcinoma of the gastric cardia. J Natl Cancer Inst 96:388–396

    Article  PubMed  Google Scholar 

  77. Yamagata H, Kiyohara Y, Aoyagi K et al (2000) Impact of Helicobacter pylori infection on gastric cancer incidence in a general Japanese population: the Hisayama study. Arch Intern Med 160:1962–1968

    Article  CAS  PubMed  Google Scholar 

  78. Kato M, Asaka M, Shimizu Y, Nobuta A, Takeda H, Sugiyama T (2004) Relationship between Helicobacter pylori infection and the prevalence, site and histological type of gastric cancer. Aliment Pharmacol Ther 20(Suppl 1):85–89

    Article  PubMed  Google Scholar 

  79. Shin A, Shin HR, Kang D, Park SK, Kim CS, Yoo KY (2005) A nested case–control study of the association of Helicobacter pylori infection with gastric adenocarcinoma in Korea. Br J Cancer 92:1273–1275

    Article  CAS  PubMed  Google Scholar 

  80. Derakhshan MH, Malekzadeh R, Watabe H et al (2008) Combination of gastric atrophy, reflux symptoms and histological subtype indicates two distinct aetiologies of gastric cardia cancer. Gut 57:298–305

    Article  CAS  PubMed  Google Scholar 

  81. Sasazuki S, Inoue M, Iwasaki M et al (2006) Effect of Helicobacter pylori infection combined with CagA and pepsinogen status on gastric cancer development among Japanese men and women: a nested case–control study. Cancer Epidemiol Biomarkers Prev 15:1341–1347

    Article  CAS  PubMed  Google Scholar 

  82. Komoto K, Haruma K, Kamada T et al (1998) Helicobacter pylori infection and gastric neoplasia: correlations with histological gastritis and tumor histology. Am J Gastroenterol 93:1271–1276

    Article  CAS  PubMed  Google Scholar 

  83. Yuan JM, Yu MC, Xu WW, Cockburn M, Gao YT, Ross RK (1999) Helicobacter pylori infection and risk of gastric cancer in Shanghai, China: updated results based upon a locally developed and validated assay and further follow-up of the cohort. Cancer Epidemiol Biomarkers Prev 8:621–624

    CAS  PubMed  Google Scholar 

  84. Yang KC, Chu A, Liao CS, Lin YM, Wang GM (2006) Evaluation of the role of H. pylori infection in pathogenesis of gastric cancer by immunoblot assay. World J Gastroenterol 12:7029–7032

    CAS  PubMed  Google Scholar 

  85. Parsonnet J, Samloff IM, Nelson LM, Orentreich N, Vogelman JH, Friedman GD (1993) Helicobacter pylori, pepsinogen, and risk for gastric adenocarcinoma. Cancer Epidemiol Biomarkers Prev 2:461–466

    CAS  PubMed  Google Scholar 

  86. Enroth H, Kraaz W, Engstrand L, Nyren O, Rohan T (2000) Helicobacter pylori strain types and risk of gastric cancer: a case–control study. Cancer Epidemiol Biomarkers Prev 9:981–985

    CAS  PubMed  Google Scholar 

  87. Zhang ZF, Kurtz RC, Klimstra DS et al (1999) Helicobacter pylori infection on the risk of stomach cancer and chronic atrophic gastritis. Cancer Detect Prev 23:357–367

    Article  CAS  PubMed  Google Scholar 

  88. Lochhead P, El-Omar EM (2007) Helicobacter pylori infection and gastric cancer. Best Pract Res Clin Gastroenterol 21:281–297

    Article  CAS  PubMed  Google Scholar 

  89. Marsman WA, Tytgat GN, ten Kate FJ, van Lanschot JJ (2005) Differences and similarities of adenocarcinomas of the esophagus and esophagogastric junction. J Surg Oncol 92:160–168

    Article  CAS  PubMed  Google Scholar 

  90. Lunet N, Azevedo A (2009) On the comparability of population-based and hospital-based case–control studies. Gac Sanit 23:564; author reply 565

    Google Scholar 

  91. Peleteiro B, Lunet N, Barros R, La Vecchia C, Barros H (2010) Factors contributing to the underestimation of Helicobacter pylori-associated gastric cancer risk in a high-prevalence population. Cancer Causes Control 21:1257–1264

    Article  PubMed  Google Scholar 

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Acknowledgments

Grants from Fundação para a Ciência e Tecnologia are gratefully acknowledged (PTDC/SAU-ESA/71517/2006 and SFRH/BD/36818/2007).

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Cavaleiro-Pinto, M., Peleteiro, B., Lunet, N. et al. Helicobacter pylori infection and gastric cardia cancer: systematic review and meta-analysis. Cancer Causes Control 22, 375–387 (2011). https://doi.org/10.1007/s10552-010-9707-2

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