Skip to main content
Top
Published in: Cancer Causes & Control 8/2010

01-08-2010 | Original paper

Factors contributing to the underestimation of Helicobacter pylori-associated gastric cancer risk in a high-prevalence population

Authors: Bárbara Peleteiro, Nuno Lunet, Rita Barros, Carlo La Vecchia, Henrique Barros

Published in: Cancer Causes & Control | Issue 8/2010

Login to get access

Abstract

Objective

This study aimed to identify sources of underestimation of the association between Helicobacter pylori infection and non-cardia gastric cancer, in a high-risk European population.

Methods

Non-cardia gastric cancer patients (n = 420) recruited in two major hospitals in North of Portugal and population controls (n = 1,389) were evaluated. Whole-cell IgG antibodies against H. pylori were quantified by ELISA and Western Blot testing was conducted in a subsample (272 cases and 186 controls) allowing for the detection of current infection marker and CagA. Sex- and age-adjusted odds ratios (OR) and 95% confidence intervals (95% CI) were computed.

Results

When assessing infection by ELISA, the OR for its association with gastric cancer decreases and reverts as IgG titers increased, from 1.96 (95% CI: 1.09–3.54) for borderline positive results (16.0–21.9 RU/ml) to 0.52 (95% CI: 0.36–0.74) for the highest IgG levels (≥102.0 RU/ml). The same pattern was observed across strata of age and blood collection timing with stronger associations among younger subjects and those providing blood samples earlier after diagnosis. The presence of CagA (Western Blot) was associated with an increased risk of gastric cancer (OR = 11.32; 95% CI: 5.64–22.73).

Conclusion

The use of methods with low sensitivity to detect past infection leads to a substantial underestimation of gastric cancer risk in high-prevalence settings.
Literature
1.
go back to reference Parkin DM (2006) The global health burden of infection-associated cancers in the year 2002. Int J Cancer 118:3030–3044CrossRefPubMed Parkin DM (2006) The global health burden of infection-associated cancers in the year 2002. Int J Cancer 118:3030–3044CrossRefPubMed
2.
go back to reference IARC (1994) Schistosomes, liver flukes and Helicobacter pylori. IARC working group on the evaluation of carcinogenic risks to humans. Lyon, 7–14 June 1994. IARC Monogr Eval Carcinog Risks Hum 61:1–241 IARC (1994) Schistosomes, liver flukes and Helicobacter pylori. IARC working group on the evaluation of carcinogenic risks to humans. Lyon, 7–14 June 1994. IARC Monogr Eval Carcinog Risks Hum 61:1–241
3.
go back to reference 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 94:2373–2379CrossRefPubMed 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 94:2373–2379CrossRefPubMed
4.
go back to reference Helicobacter and Cancer Collaborative Group (2001) Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut 49:347–353CrossRef Helicobacter and Cancer Collaborative Group (2001) Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut 49:347–353CrossRef
5.
go back to reference Xue FB, Xu YY, Wan Y, Pan BR, Ren J, Fan DM (2001) Association of H. pylori infection with gastric carcinoma: a meta analysis. World J Gastroenterol 7:801–804PubMed Xue FB, Xu YY, Wan Y, Pan BR, Ren J, Fan DM (2001) Association of H. pylori infection with gastric carcinoma: a meta analysis. World J Gastroenterol 7:801–804PubMed
6.
go back to reference Webb PM, Yu MC, Forman D, Henderson BE, Newell DG, Yuan JM, Gao YT, Ross RK (1996) An apparent lack of association between Helicobacter pylori infection and risk of gastric cancer in China. Int J Cancer 67:603–607CrossRefPubMed Webb PM, Yu MC, Forman D, Henderson BE, Newell DG, Yuan JM, Gao YT, Ross RK (1996) An apparent lack of association between Helicobacter pylori infection and risk of gastric cancer in China. Int J Cancer 67:603–607CrossRefPubMed
7.
go back to reference Kato S, Onda M, Matsukura N, Tokunaga A, Matsuda N, Yamashita K, Shields PG (1996) Genetic polymorphisms of the cancer related gene and Helicobacter pylori infection in Japanese gastric cancer patients. An age and gender matched case–control study. Cancer 77:1654–1661PubMed Kato S, Onda M, Matsukura N, Tokunaga A, Matsuda N, Yamashita K, Shields PG (1996) Genetic polymorphisms of the cancer related gene and Helicobacter pylori infection in Japanese gastric cancer patients. An age and gender matched case–control study. Cancer 77:1654–1661PubMed
8.
go back to reference Fukuda H, Saito D, Hayashi S, Hisai H, Ono H, Yoshida S, Oguro Y, Noda T, Sato T, Katoh M et al (1995) Helicobacter pylori infection, serum pepsinogen level and gastric cancer: a case–control study in Japan. Jpn J Cancer Res 86:64–71PubMed Fukuda H, Saito D, Hayashi S, Hisai H, Ono H, Yoshida S, Oguro Y, Noda T, Sato T, Katoh M et al (1995) Helicobacter pylori infection, serum pepsinogen level and gastric cancer: a case–control study in Japan. Jpn J Cancer Res 86:64–71PubMed
9.
go back to reference Blaser MJ, Kobayashi K, Cover TL, Cao P, Feurer ID, Perez-Perez GI (1993) Helicobacter pylori infection in Japanese patients with adenocarcinoma of the stomach. Int J Cancer 55:799–802CrossRefPubMed Blaser MJ, Kobayashi K, Cover TL, Cao P, Feurer ID, Perez-Perez GI (1993) Helicobacter pylori infection in Japanese patients with adenocarcinoma of the stomach. Int J Cancer 55:799–802CrossRefPubMed
10.
go back to reference Tatsuta M, Iishi H, Okuda S, Taniguchi H, Yokota Y (1993) The association of Helicobacter pylori with differentiated-type early gastric cancer. Cancer 72:1841–1845CrossRefPubMed Tatsuta M, Iishi H, Okuda S, Taniguchi H, Yokota Y (1993) The association of Helicobacter pylori with differentiated-type early gastric cancer. Cancer 72:1841–1845CrossRefPubMed
11.
go back to reference Azuma T, Ito S, Sato F, Yamazaki Y, Miyaji H, Ito Y, Suto H, Kuriyama M, Kato T, Kohli Y (1998) The role of the HLA-DQA1 gene in resistance to atrophic gastritis and gastric adenocarcinoma induced by Helicobacter pylori infection. Cancer 82:1013–1018CrossRefPubMed Azuma T, Ito S, Sato F, Yamazaki Y, Miyaji H, Ito Y, Suto H, Kuriyama M, Kato T, Kohli Y (1998) The role of the HLA-DQA1 gene in resistance to atrophic gastritis and gastric adenocarcinoma induced by Helicobacter pylori infection. Cancer 82:1013–1018CrossRefPubMed
12.
go back to reference Shibata T, Imoto I, Ohuchi Y, Taguchi Y, Takaji S, Ikemura N, Nakao K, Shima T (1996) Helicobacter pylori infection in patients with gastric carcinoma in biopsy and surgical resection specimens. Cancer 77:1044–1049CrossRefPubMed Shibata T, Imoto I, Ohuchi Y, Taguchi Y, Takaji S, Ikemura N, Nakao K, Shima T (1996) Helicobacter pylori infection in patients with gastric carcinoma in biopsy and surgical resection specimens. Cancer 77:1044–1049CrossRefPubMed
13.
go back to reference 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 10:3278–3283PubMed 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 10:3278–3283PubMed
14.
go back to reference 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 92:1273–1275CrossRefPubMed 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 92:1273–1275CrossRefPubMed
15.
go back to reference Watabe H, Mitsushima T, Yamaji Y, Okamoto M, Wada R, Kokubo T, Doi H, Yoshida H, Kawabe T, Omata M (2005) Predicting the development of gastric cancer from combining Helicobacter pylori antibodies and serum pepsinogen status: a prospective endoscopic cohort study. Gut 54:764–768CrossRefPubMed Watabe H, Mitsushima T, Yamaji Y, Okamoto M, Wada R, Kokubo T, Doi H, Yoshida H, Kawabe T, Omata M (2005) Predicting the development of gastric cancer from combining Helicobacter pylori antibodies and serum pepsinogen status: a prospective endoscopic cohort study. Gut 54:764–768CrossRefPubMed
16.
go back to reference Huang JQ, Sridhar S, Chen Y, Hunt RH (1998) Meta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer. Gastroenterology 114:1169–1179CrossRefPubMed Huang JQ, Sridhar S, Chen Y, Hunt RH (1998) Meta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer. Gastroenterology 114:1169–1179CrossRefPubMed
17.
go back to reference 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 159:252–258CrossRefPubMed 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 159:252–258CrossRefPubMed
18.
go back to reference 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 121:784–791CrossRefPubMed 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 121:784–791CrossRefPubMed
19.
go back to reference Lunet N, Barros H (2006) Helicobacter pylori infection and gastric cancer in developing countries: revisiting the “enigmas”. In: Ly A, Khayat D (eds) About cancer in Africa: from epidemiology to biomedical applications and perspectives. INCa, Paris, pp 257–272 Lunet N, Barros H (2006) Helicobacter pylori infection and gastric cancer in developing countries: revisiting the “enigmas”. In: Ly A, Khayat D (eds) About cancer in Africa: from epidemiology to biomedical applications and perspectives. INCa, Paris, pp 257–272
20.
go back to reference Weck MN, Gao L, Brenner H (2009) Helicobacter pylori infection and chronic atrophic gastritis: associations according to severity of disease. Epidemiology 20:569–574CrossRefPubMed Weck MN, Gao L, Brenner H (2009) Helicobacter pylori infection and chronic atrophic gastritis: associations according to severity of disease. Epidemiology 20:569–574CrossRefPubMed
21.
go back to reference Lunet N, Pina F, Barros H (2004) Regional trends in Portuguese gastric cancer mortality (1984–1999). Eur J Cancer Prev 13:271–275CrossRefPubMed Lunet N, Pina F, Barros H (2004) Regional trends in Portuguese gastric cancer mortality (1984–1999). Eur J Cancer Prev 13:271–275CrossRefPubMed
22.
go back to reference Lunet N, Valbuena C, Carneiro F, Lopes C, Barros H (2006) Antioxidant vitamins and risk of gastric cancer: a case–control study in Portugal. Nutr Cancer 55:71–77CrossRefPubMed Lunet N, Valbuena C, Carneiro F, Lopes C, Barros H (2006) Antioxidant vitamins and risk of gastric cancer: a case–control study in Portugal. Nutr Cancer 55:71–77CrossRefPubMed
23.
go back to reference Lunet N, Valbuena C, Vieira AL, Lopes C, David L, Carneiro F, Barros H (2007) Fruit and vegetable consumption and gastric cancer by location and histological type: case–control and meta-analysis. Eur J Cancer Prev 16:312–327CrossRefPubMed Lunet N, Valbuena C, Vieira AL, Lopes C, David L, Carneiro F, Barros H (2007) Fruit and vegetable consumption and gastric cancer by location and histological type: case–control and meta-analysis. Eur J Cancer Prev 16:312–327CrossRefPubMed
24.
go back to reference Ramos E, Lopes C, Barros H (2004) Investigating the effect of nonparticipation using a population-based case–control study on myocardial infarction. Ann Epidemiol 14:437–441CrossRefPubMed Ramos E, Lopes C, Barros H (2004) Investigating the effect of nonparticipation using a population-based case–control study on myocardial infarction. Ann Epidemiol 14:437–441CrossRefPubMed
25.
go back to reference Gal DL, Santos AC, Barros H (2005) Leisure-time versus full-day energy expenditure: a cross-sectional study of sedentarism in a Portuguese urban population. BMC Public Health 5:16CrossRefPubMed Gal DL, Santos AC, Barros H (2005) Leisure-time versus full-day energy expenditure: a cross-sectional study of sedentarism in a Portuguese urban population. BMC Public Health 5:16CrossRefPubMed
26.
go back to reference Estevens J, Fidalgo P, Tendeiro T, Chagas C, Ferra A, Leitao CN, Mira FC (1993) Anti-Helicobacter pylori antibodies prevalence and gastric adenocarcinoma in Portugal: report of a case–control study. Eur J Cancer Prev 2:377–380CrossRefPubMed Estevens J, Fidalgo P, Tendeiro T, Chagas C, Ferra A, Leitao CN, Mira FC (1993) Anti-Helicobacter pylori antibodies prevalence and gastric adenocarcinoma in Portugal: report of a case–control study. Eur J Cancer Prev 2:377–380CrossRefPubMed
27.
go back to reference 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 34:353–360CrossRefPubMed 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 34:353–360CrossRefPubMed
28.
go back to reference Klaamas K, Held M, Wadstrom T, Lipping A, Kurtenkov O (1996) IgG immune response to Helicobacter pylori antigens in patients with gastric cancer as defined by ELISA and immunoblotting. Int J Cancer 67:1–5CrossRefPubMed Klaamas K, Held M, Wadstrom T, Lipping A, Kurtenkov O (1996) IgG immune response to Helicobacter pylori antigens in patients with gastric cancer as defined by ELISA and immunoblotting. Int J Cancer 67:1–5CrossRefPubMed
29.
go back to reference Kuipers EJ (1999) Review article: exploring the link between Helicobacter pylori and gastric cancer. Aliment Pharmacol Ther 13(Suppl 1):3–11CrossRefPubMed Kuipers EJ (1999) Review article: exploring the link between Helicobacter pylori and gastric cancer. Aliment Pharmacol Ther 13(Suppl 1):3–11CrossRefPubMed
30.
go back to reference Correa P, Haenszel W, Cuello C, Tannenbaum S, Archer M (1975) A model for gastric cancer epidemiology. Lancet 2:58–60CrossRefPubMed Correa P, Haenszel W, Cuello C, Tannenbaum S, Archer M (1975) A model for gastric cancer epidemiology. Lancet 2:58–60CrossRefPubMed
31.
go back to reference 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 (2004) Progression of chronic atrophic gastritis associated with Helicobacter pylori infection increases risk of gastric cancer. Int J Cancer 109:138–143CrossRefPubMed 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 (2004) Progression of chronic atrophic gastritis associated with Helicobacter pylori infection increases risk of gastric cancer. Int J Cancer 109:138–143CrossRefPubMed
32.
go back to reference Weck MN, Stegmaier C, Rothenbacher D, Brenner H (2007) Epidemiology of chronic atrophic gastritis: population-based study among 9,444 older adults from Germany. Aliment Pharmacol Ther 26:879–887PubMedCrossRef Weck MN, Stegmaier C, Rothenbacher D, Brenner H (2007) Epidemiology of chronic atrophic gastritis: population-based study among 9,444 older adults from Germany. Aliment Pharmacol Ther 26:879–887PubMedCrossRef
33.
go back to reference Yanaoka K, Oka M, Mukoubayashi C, Yoshimura N, Enomoto S, Iguchi M, Magari H, Utsunomiya H, Tamai H, Arii K, Ohata H, Fujishiro M, Takeshita T, Mohara O, Ichinose M (2008) Cancer high-risk subjects identified by serum pepsinogen tests: outcomes after 10-year follow-up in asymptomatic middle-aged males. Cancer Epidemiol Biomarkers Prev 17:838–845CrossRefPubMed Yanaoka K, Oka M, Mukoubayashi C, Yoshimura N, Enomoto S, Iguchi M, Magari H, Utsunomiya H, Tamai H, Arii K, Ohata H, Fujishiro M, Takeshita T, Mohara O, Ichinose M (2008) Cancer high-risk subjects identified by serum pepsinogen tests: outcomes after 10-year follow-up in asymptomatic middle-aged males. Cancer Epidemiol Biomarkers Prev 17:838–845CrossRefPubMed
34.
go back to reference Katsube T, Ogawa K, Hamaguchi K, Murayama M, Konnno S, Shimakawa T, Naritaka Y, Yagawa H, Kajiwara T, Aiba M (2002) Prevalence of Helicobacter pylori in the residual stomach after gastrectomy for gastric cancer. Hepatogastroenterology 49:128–132PubMed Katsube T, Ogawa K, Hamaguchi K, Murayama M, Konnno S, Shimakawa T, Naritaka Y, Yagawa H, Kajiwara T, Aiba M (2002) Prevalence of Helicobacter pylori in the residual stomach after gastrectomy for gastric cancer. Hepatogastroenterology 49:128–132PubMed
35.
go back to reference Kuipers EJ, Pena AS, van Kamp G, Uyterlinde AM, Pals G, Pels NF, Kurz-Pohlmann E, Meuwissen SG (1993) Seroconversion for Helicobacter pylori. Lancet 342:328–331CrossRefPubMed Kuipers EJ, Pena AS, van Kamp G, Uyterlinde AM, Pals G, Pels NF, Kurz-Pohlmann E, Meuwissen SG (1993) Seroconversion for Helicobacter pylori. Lancet 342:328–331CrossRefPubMed
36.
go back to reference Sasazuki S, Inoue M, Iwasaki M, Otani T, Yamamoto S, Ikeda S, Hanaoka T, Tsugane S (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 15:1341–1347CrossRefPubMed Sasazuki S, Inoue M, Iwasaki M, Otani T, Yamamoto S, Ikeda S, Hanaoka T, Tsugane S (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 15:1341–1347CrossRefPubMed
37.
go back to reference 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 42:933–940CrossRefPubMed 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 42:933–940CrossRefPubMed
38.
go back to reference Mitchell H, English DR, Elliott F, Gengos M, Barrett JH, Giles GG, Forman D (2008) Immunoblotting using multiple antigens is essential to demonstrate the true risk of Helicobacter pylori infection for gastric cancer. Aliment Pharmacol Ther 28:903–910PubMed Mitchell H, English DR, Elliott F, Gengos M, Barrett JH, Giles GG, Forman D (2008) Immunoblotting using multiple antigens is essential to demonstrate the true risk of Helicobacter pylori infection for gastric cancer. Aliment Pharmacol Ther 28:903–910PubMed
39.
go back to reference Sorberg M, Engstrand L, Strom M, Jonsson KA, Jorbeck H, Granstrom M (1997) The diagnostic value of enzyme immunoassay and immunoblot in monitoring eradication of Helicobacter pylori. Scand J Infect Dis 29:147–151CrossRefPubMed Sorberg M, Engstrand L, Strom M, Jonsson KA, Jorbeck H, Granstrom M (1997) The diagnostic value of enzyme immunoassay and immunoblot in monitoring eradication of Helicobacter pylori. Scand J Infect Dis 29:147–151CrossRefPubMed
40.
go back to reference Romero-Gallo J, Perez-Perez GI, Novick RP, Kamath P, Norbu T, Blaser MJ (2002) Responses of endoscopy patients in Ladakh, India, to Helicobacter pylori whole-cell and Cag A antigens. Clin Diagn Lab Immunol 9:1313–1317PubMed Romero-Gallo J, Perez-Perez GI, Novick RP, Kamath P, Norbu T, Blaser MJ (2002) Responses of endoscopy patients in Ladakh, India, to Helicobacter pylori whole-cell and Cag A antigens. Clin Diagn Lab Immunol 9:1313–1317PubMed
41.
go back to reference Lu CY, Kuo CH, Lo YC, Chuang HY, Yang YC, Wu IC, Yu FJ, Lee YC, Jan CM, Wang WM, Wu DC (2005) The best method of detecting prior Helicobacter pylori infection. World J Gastroenterol 11:5672–5676PubMed Lu CY, Kuo CH, Lo YC, Chuang HY, Yang YC, Wu IC, Yu FJ, Lee YC, Jan CM, Wang WM, Wu DC (2005) The best method of detecting prior Helicobacter pylori infection. World J Gastroenterol 11:5672–5676PubMed
42.
go back to reference Rahman SH, Azam MG, Rahman MA, Arfin MS, Alam MM, Bhuiyan TM, Ahmed N, Rahman M, Nahar S, Hassan MS (2008) Non-invasive diagnosis of H. pylori infection: evaluation of serological tests with and without current infection marker CIM. World J Gastroenterol 14:1231–1236CrossRefPubMed Rahman SH, Azam MG, Rahman MA, Arfin MS, Alam MM, Bhuiyan TM, Ahmed N, Rahman M, Nahar S, Hassan MS (2008) Non-invasive diagnosis of H. pylori infection: evaluation of serological tests with and without current infection marker CIM. World J Gastroenterol 14:1231–1236CrossRefPubMed
43.
go back to reference Veijola L, Oksanen A, Sipponen P, Rautelin H (2008) Evaluation of a commercial immunoblot, Helicoblot 2.1, for diagnosis of Helicobacter pylori infection. Clin Vaccine Immunol 15:1705–1710CrossRefPubMed Veijola L, Oksanen A, Sipponen P, Rautelin H (2008) Evaluation of a commercial immunoblot, Helicoblot 2.1, for diagnosis of Helicobacter pylori infection. Clin Vaccine Immunol 15:1705–1710CrossRefPubMed
44.
go back to reference Xia HH, Talley NJ (1997) Natural acquisition and spontaneous elimination of Helicobacter pylori infection: clinical implications. Am J Gastroenterol 92:1780–1787PubMed Xia HH, Talley NJ (1997) Natural acquisition and spontaneous elimination of Helicobacter pylori infection: clinical implications. Am J Gastroenterol 92:1780–1787PubMed
45.
go back to reference Lunet N, Barros H (2003) Helicobacter pylori infection and gastric cancer: facing the enigmas. Int J Cancer 106:953–960CrossRefPubMed Lunet N, Barros H (2003) Helicobacter pylori infection and gastric cancer: facing the enigmas. Int J Cancer 106:953–960CrossRefPubMed
46.
go back to reference Rothenbacher D, Brenner H (2003) Burden of Helicobacter pylori and H. pylori-related diseases in developed countries: recent developments and future implications. Microbes Infect 5:693–703CrossRefPubMed Rothenbacher D, Brenner H (2003) Burden of Helicobacter pylori and H. pylori-related diseases in developed countries: recent developments and future implications. Microbes Infect 5:693–703CrossRefPubMed
47.
go back to reference Hansson LR, Engstrand L, Nyren O, Lindgren A (1995) Prevalence of Helicobacter pylori infection in subtypes of gastric cancer. Gastroenterology 109:885–888CrossRefPubMed Hansson LR, Engstrand L, Nyren O, Lindgren A (1995) Prevalence of Helicobacter pylori infection in subtypes of gastric cancer. Gastroenterology 109:885–888CrossRefPubMed
48.
go back to reference Plummer M, van Doorn LJ, Franceschi S, Kleter B, Canzian F, Vivas J, Lopez G, Colin D, Munoz N, Kato I (2007) Helicobacter pylori cytotoxin-associated genotype and gastric precancerous lesions. J Natl Cancer Inst 99:1328–1334CrossRefPubMed Plummer M, van Doorn LJ, Franceschi S, Kleter B, Canzian F, Vivas J, Lopez G, Colin D, Munoz N, Kato I (2007) Helicobacter pylori cytotoxin-associated genotype and gastric precancerous lesions. J Natl Cancer Inst 99:1328–1334CrossRefPubMed
49.
go back to reference Huang JQ, Zheng GF, Sumanac K, Irvine EJ, Hunt RH (2003) Meta-analysis of the relationship between cagA seropositivity and gastric cancer. Gastroenterology 125:1636–1644CrossRefPubMed Huang JQ, Zheng GF, Sumanac K, Irvine EJ, Hunt RH (2003) Meta-analysis of the relationship between cagA seropositivity and gastric cancer. Gastroenterology 125:1636–1644CrossRefPubMed
50.
go back to reference Gisbert JP, Blanco M, Benito LM, Pajares JM (2000) Value of quantitative serology for confirmation of Helicobacter pylori eradication: an 18-month follow-up study. Clin Infect Dis 30:976–980CrossRefPubMed Gisbert JP, Blanco M, Benito LM, Pajares JM (2000) Value of quantitative serology for confirmation of Helicobacter pylori eradication: an 18-month follow-up study. Clin Infect Dis 30:976–980CrossRefPubMed
51.
go back to reference Herbrink P, van Doorn LJ (2000) Serological methods for diagnosis of Helicobacter pylori infection and monitoring of eradication therapy. Eur J Clin Microbiol Infect Dis 19:164–173CrossRefPubMed Herbrink P, van Doorn LJ (2000) Serological methods for diagnosis of Helicobacter pylori infection and monitoring of eradication therapy. Eur J Clin Microbiol Infect Dis 19:164–173CrossRefPubMed
52.
go back to reference Mitchell HM, Ally R, Wadee A, Wiseman M, Segal I (2002) Major differences in the IgG subclass response to Helicobacter pylori in the first and third worlds. Scand J Gastroenterol 37:517–522CrossRefPubMed Mitchell HM, Ally R, Wadee A, Wiseman M, Segal I (2002) Major differences in the IgG subclass response to Helicobacter pylori in the first and third worlds. Scand J Gastroenterol 37:517–522CrossRefPubMed
53.
go back to reference Campbell DI, Pearce MS, Parker L, Thomas JE, Sullivan PB, Dale A (2004) Immunoglobulin G subclass responses to Helicobacter pylori vary with age in populations with different levels of risk of gastric carcinoma. Clin Diagn Lab Immunol 11:631–633PubMed Campbell DI, Pearce MS, Parker L, Thomas JE, Sullivan PB, Dale A (2004) Immunoglobulin G subclass responses to Helicobacter pylori vary with age in populations with different levels of risk of gastric carcinoma. Clin Diagn Lab Immunol 11:631–633PubMed
54.
go back to reference Mbulaiteye SM, Gold BD, Pfeiffer RM, Brubaker GR, Shao J, Biggar RJ, Hisada M (2006) H. pylori-infection and antibody immune response in a rural Tanzanian population. Infect Agent Cancer 1:3CrossRefPubMed Mbulaiteye SM, Gold BD, Pfeiffer RM, Brubaker GR, Shao J, Biggar RJ, Hisada M (2006) H. pylori-infection and antibody immune response in a rural Tanzanian population. Infect Agent Cancer 1:3CrossRefPubMed
Metadata
Title
Factors contributing to the underestimation of Helicobacter pylori-associated gastric cancer risk in a high-prevalence population
Authors
Bárbara Peleteiro
Nuno Lunet
Rita Barros
Carlo La Vecchia
Henrique Barros
Publication date
01-08-2010
Publisher
Springer Netherlands
Published in
Cancer Causes & Control / Issue 8/2010
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-010-9553-2

Other articles of this Issue 8/2010

Cancer Causes & Control 8/2010 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine