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[Cancer Research 55, 2111-2115, May 15, 1995]
© 1995 American Association for Cancer Research
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Infection with Helicobacter pylori Strains Possessing cagA Is Associated with an Increased Risk of Developing Adenocarcinoma of the Stomach1

Martin J. Blaser2, Guillermo I. Perez-Perez, Harry Kleanthous, Timothy L. Cover, Richard M. Peek, P. H. Chyou, Grant N. Stemmermann and Abraham Nomura

Departments of Medicine [M. J. B., G. I. P-P., T. L. C., R. M. P.] and Microbiology and Immunology [M. J. B.], Vanderbilt University School of Medicine, Nashville, Tennessee 37232; Medical Service, Department of Veterans Affairs Medical Center, Nashville, Tennessee 37212 [M. J. B., T. L. C.]; OraVax, Inc., Cambridge, Massachusetts 02139 [H. K.]; and Japan-Hawaii Cancer Study, Honolulu, Hawaii 96817 [P. H. C., G. N. S., A. N.]

To determine whether infection with a Helicobacter pylori strain possessing cagA is associated with an increased risk of development of adenocarcinoma of the stomach, we used a nested case-control study based on a cohort of 5443 Japanese-American men in Oahu, Hawaii, who had a physical examination and a phlebotomy during 1967 to 1970. We matched 103 H. pylori-infected men who developed gastric cancer during a 21-year surveillence period with 103 H. pylori-infected men who did not develop gastric cancer and tested stored serum specimens from patients and controls for the presence of serum IgG to the cagA product of H. pylori using an ELISA. The serum IgG assay using a recombinant CagA fragment had a sensitivity of 94.4% and a specificity of 92.5% when used in a clinically defined population; serological results were stable for more than 7 years. For men with antibodies to CagA, the odds ratio of developing gastric cancer was 1.9 (95% confidence interval, 0.9–4.0); for intestinal type cancer of the distal stomach, the odds ratio was 2.3 (95% confidence interval, 1.0–5.2). Age <72 years and advanced tumor stage at diagnosis were significantly associated with CagA seropositivity. We conclude that infection with a cagA-positive H. pylori strain in comparison with a cagA-negative strain somewhat increases the risk for development of gastric cancer, especially intestinal type affecting the distal stomach.

1 Supported by NIH Grants R01CA 58834 and 33644, R29DK45293, and 5T32DK07673, and the Medical Research Service of the Department of Veterans Affairs.

2 To whom requests for reprints should be addressed, at Division of Infectious Diseases, Vanderbilt University School of Medicine, A-3310 Medical Center North, 1161 21st Avenue South, Nashville, TN 37232-2605.

Received 1/24/95. Accepted 3/16/95.




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K. Yokoyama, H. Higashi, S. Ishikawa, Y. Fujii, S. Kondo, H. Kato, T. Azuma, A. Wada, T. Hirayama, H. Aburatani, et al.
Functional antagonism between Helicobacter pylori CagA and vacuolating toxin VacA in control of the NFAT signaling pathway in gastric epithelial cells
PNAS, July 5, 2005; 102(27): 9661 - 9666.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. Higashi, K. Yokoyama, Y. Fujii, S. Ren, H. Yuasa, I. Saadat, N. Murata-Kamiya, T. Azuma, and M. Hatakeyama
EPIYA Motif Is a Membrane-targeting Signal of Helicobacter pylori Virulence Factor CagA in Mammalian Cells
J. Biol. Chem., June 17, 2005; 280(24): 23130 - 23137.
[Abstract] [Full Text] [PDF]

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 Infect. Immun.Home page
C. E. Terry, L. M. McGinnis, K. C. Madigan, P. Cao, T. L. Cover, G. W. Liechti, R. M. Peek Jr., and M. H. Forsyth
Genomic Comparison of cag Pathogenicity Island (PAI)-Positive and -Negative Helicobacter pylori Strains: Identification of Novel Markers for cag PAI-Positive Strains
Infect. Immun., June 1, 2005; 73(6): 3794 - 3798.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
C. Ghose, G. I. Perez-Perez, L. J. van Doorn, M. G. Dominguez-Bello, and M. J. Blaser
High Frequency of Gastric Colonization with Multiple Helicobacter pylori Strains in Venezuelan Subjects
J. Clin. Microbiol., June 1, 2005; 43(6): 2635 - 2641.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
C.-C. Wu, P.-Y. Chou, C.-T. Hu, Z.-C. Liu, C.-Y. Lin, Y.-H. Tseng, and N.-T. Lin
Clinical Relevance of the vacA, iceA, cagA, and flaA Genes of Helicobacter pylori Strains Isolated in Eastern Taiwan
J. Clin. Microbiol., June 1, 2005; 43(6): 2913 - 2915.
[Abstract] [Full Text] [PDF]

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 GutHome page
H Saito, Y Yamaoka, S Ishizone, F Maruta, A Sugiyama, D Y Graham, K Yamauchi, H Ota, and S Miyagawa
Roles of virD4 and cagG genes in the cag pathogenicity island of Helicobacter pylori using a Mongolian gerbil model
Gut, May 1, 2005; 54(5): 584 - 590.
[Abstract] [Full Text] [PDF]

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 Sci SignalHome page
R. M. Peek Jr.
Orchestration of Aberrant Epithelial Signaling by Helicobacter pylori CagA
Sci. Signal., March 29, 2005; 2005(277): pe14 - pe14.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
Y. Zhang, R. H. Argent, D. P. Letley, R. J. Thomas, and J. C. Atherton
Tyrosine Phosphorylation of CagA from Chinese Helicobacter pylori Isolates in AGS Gastric Epithelial Cells
J. Clin. Microbiol., February 1, 2005; 43(2): 786 - 790.
[Abstract] [Full Text] [PDF]

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 CVIHome page
J. H. Siman, L. Engstrand, G. Berglund, C.-H. Floren, and A. Forsgren
Evaluation of Western Blot CagA Seropositivity in Helicobacter pylori-Seropositive and -Seronegative Subjects
Clin. Vaccine Immunol., February 1, 2005; 12(2): 304 - 309.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
G. Cui, T. J. Koh, D. Chen, C.-M. Zhao, S. Takaishi, G. J. Dockray, A. Varro, A. B. Rogers, J. G. Fox, and T. C. Wang
Overexpression of Glycine-Extended Gastrin Inhibits Parietal Cell Loss and Atrophy in the Mouse Stomach
Cancer Res., November 15, 2004; 64(22): 8160 - 8166.
[Abstract] [Full Text] [PDF]

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 Infect. Immun.Home page
L. J. Thompson, S. J. Danon, J. E. Wilson, J. L. O'Rourke, N. R. Salama, S. Falkow, H. Mitchell, and A. Lee
Chronic Helicobacter pylori Infection with Sydney Strain 1 and a Newly Identified Mouse-Adapted Strain (Sydney Strain 2000) in C57BL/6 and BALB/c Mice
Infect. Immun., August 1, 2004; 72(8): 4668 - 4679.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
K.-H. Lee, M.-J. Cho, Y. Yamaoka, D. Y. Graham, Y.-J. Yun, S.-Y. Woo, C.-Y. Lim, K.-S. Ko, B.-J. Kim, H.-C. Jung, et al.
Alanine-Threonine Polymorphism of Helicobacter pylori RpoB Is Correlated with Differential Induction of Interleukin-8 in MKN45 Cells
J. Clin. Microbiol., August 1, 2004; 42(8): 3518 - 3524.
[Abstract] [Full Text] [PDF]

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 GutHome page
R Rad, A Dossumbekova, B Neu, R Lang, S Bauer, D Saur, M Gerhard, and C Prinz
Cytokine gene polymorphisms influence mucosal cytokine expression, gastric inflammation, and host specific colonisation during Helicobacter pylori infection
Gut, August 1, 2004; 53(8): 1082 - 1089.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
T. Azuma, A. Yamakawa, S. Yamazaki, M. Ohtani, Y. Ito, A. Muramatsu, H. Suto, Y. Yamazaki, Y. Keida, H. Higashi, et al.
Distinct Diversity of the cag Pathogenicity Island among Helicobacter pylori Strains in Japan
J. Clin. Microbiol., June 1, 2004; 42(6): 2508 - 2517.
[Abstract] [Full Text] [PDF]

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 GutHome page
H Eguchi, S Carpentier, S S Kim, and S F Moss
p27kip1 regulates the apoptotic response of gastric epithelial cells to Helicobacter pylori
Gut, June 1, 2004; 53(6): 797 - 804.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
E. E. Schneeberger and R. D. Lynch
The tight junction: a multifunctional complex
Am J Physiol Cell Physiol, June 1, 2004; 286(6): C1213 - C1228.
[Abstract] [Full Text] [PDF]

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 Infect. Immun.Home page
R. J. Menaker, P. J. M. Ceponis, and N. L. Jones
Helicobacter pylori Induces Apoptosis of Macrophages in Association with Alterations in the Mitochondrial Pathway
Infect. Immun., May 1, 2004; 72(5): 2889 - 2898.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. Higashi, A. Nakaya, R. Tsutsumi, K. Yokoyama, Y. Fujii, S. Ishikawa, M. Higuchi, A. Takahashi, Y. Kurashima, Y. Teishikata, et al.
Helicobacter pylori CagA Induces Ras-independent Morphogenetic Response through SHP-2 Recruitment and Activation
J. Biol. Chem., April 23, 2004; 279(17): 17205 - 17216.
[Abstract] [Full Text] [PDF]

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 J Med MicrobiolHome page
J. Zhou, J. Zhang, C. Xu, and L. He
cagA genotype and variants in Chinese Helicobacter pylori strains and relationship to gastroduodenal diseases
J. Med. Microbiol., March 1, 2004; 53(3): 231 - 235.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
I. M. Carroll, N. Ahmed, S. M. Beesley, A. A. Khan, S. Ghousunnissa, C. A. O Morain, and C. J. Smyth
Fine-Structure Molecular Typing of Irish Helicobacter pylori Isolates and Their Genetic Relatedness to Strains from Four Different Continents
J. Clin. Microbiol., December 1, 2003; 41(12): 5755 - 5759.
[Abstract] [Full Text] [PDF]

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 JEMHome page
R. A. Aras, W. Fischer, G. I. Perez-Perez, M. Crosatti, T. Ando, R. Haas, and M. J. Blaser
Plasticity of Repetitive DNA Sequences within a Bacterial (Type IV) Secretion System Component
J. Exp. Med., November 3, 2003; 198(9): 1349 - 1360.
[Abstract] [Full Text] [PDF]

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 CVIHome page
R.-K. Vilaichone, V. Mahachai, C. Kositchaiwat, D. Y. Graham, and Y. Yamaoka
Relation between Seroreactivity to Low-Molecular-Weight Helicobacter pylori-Specific Antigens and Disease Presentation
Clin. Vaccine Immunol., November 1, 2003; 10(6): 1025 - 1028.
[Abstract] [Full Text] [PDF]

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 HeartHome page
D Tousoulis, G Davies, C Stefanadis, P Toutouzas, and J A Ambrose
Inflammatory and thrombotic mechanisms in coronary atherosclerosis
Heart, September 1, 2003; 89(9): 993 - 997.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
A. G. Oliveira, A. Santos, J. B. Guerra, G. A. Rocha, A. M. C. Rocha, C. A. Oliveira, M. M. D. A. Cabral, A. M. M. F. Nogueira, and D. M. M. Queiroz
babA2- and cagA-Positive Helicobacter pylori Strains Are Associated with Duodenal Ulcer and Gastric Carcinoma in Brazil
J. Clin. Microbiol., August 1, 2003; 41(8): 3964 - 3966.
[Abstract] [Full Text] [PDF]

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 J. Am. Coll. Nutr.Home page
J. A. Simon, E. S. Hudes, and G. I. Perez-Perez
Relation of Serum Ascorbic Acid to Helicobacter pylori Serology in US Adults: the Third National Health and Nutrition Examination Survey
J. Am. Coll. Nutr., August 1, 2003; 22(4): 283 - 289.
[Abstract] [Full Text] [PDF]

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 Am. J. Clin. Nutr.Home page
R. Z Stolzenberg-Solomon, K. W Dodd, M. J Blaser, J. Virtamo, P. R Taylor, and D. Albanes
Tooth loss, pancreatic cancer, and Helicobacter pylori
Am. J. Clinical Nutrition, July 1, 2003; 78(1): 176 - 181.
[Abstract] [Full Text] [PDF]

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 Infect. Immun.Home page
N. Mori, A. M. Krensky, R. Geleziunas, A. Wada, T. Hirayama, C. Sasakawa, and N. Yamamoto
Helicobacter pylori Induces RANTES through Activation of NF-{kappa}B
Infect. Immun., July 1, 2003; 71(7): 3748 - 3756.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
C.-Y. Park, M. Kwak, O. Gutierrez, D. Y. Graham, and Y. Yamaoka
Comparison of Genotyping Helicobacter pylori Directly from Biopsy Specimens and Genotyping from Bacterial Cultures
J. Clin. Microbiol., July 1, 2003; 41(7): 3336 - 3338.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
G. I. Perez-Perez, R. B. Sack, R. Reid, M. Santosham, J. Croll, and M. J. Blaser
Transient and Persistent Helicobacter pylori Colonization in Native American Children
J. Clin. Microbiol., June 1, 2003; 41(6): 2401 - 2407.
[Abstract] [Full Text] [PDF]

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 ScienceHome page
M. R. Amieva, R. Vogelmann, A. Covacci, L. S. Tompkins, W. J. Nelson, and S. Falkow
Disruption of the Epithelial Apical-Junctional Complex by Helicobacter pylori CagA
Science, May 30, 2003; 300(5624): 1430 - 1434.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
F. Kamangar, P. Limburg, P. Taylor, and S. Dawsey
Re: Helicobacter pylori and Interleukin 1 Genotyping: An Opportunity to Identify High-Risk Individuals for Gastric Carcinoma
J Natl Cancer Inst, May 21, 2003; 95(10): 760 - 760.
[Full Text] [PDF]

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 Nucleic Acids ResHome page
I. G. Boneca, H. d. Reuse, J.-C. Epinat, M. Pupin, A. Labigne, and I. Moszer
A revised annotation and comparative analysis of Helicobacter pylori genomes
Nucleic Acids Res., March 15, 2003; 31(6): 1704 - 1714.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
M. L. Tomasini, S. Zanussi, M. Sozzi, R. Tedeschi, G. Basaglia, and P. De Paoli
Heterogeneity of cag Genotypes in Helicobacterpylori Isolates from Human Biopsy Specimens
J. Clin. Microbiol., March 1, 2003; 41(3): 976 - 980.
[Abstract] [Full Text] [PDF]

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 MicrobiologyHome page
K. R. Hardie, C. Cooksley, A. D. Green, and K. Winzer
Autoinducer 2 activity in Escherichia coli culture supernatants can be actively reduced despite maintenance of an active synthase, LuxS
Microbiology, March 1, 2003; 149(3): 715 - 728.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. Tsutsumi, H. Higashi, M. Higuchi, M. Okada, and M. Hatakeyama
Attenuation of Helicobacter pylori CagA{middle dot}SHP-2 Signaling by Interaction between CagA and C-terminal Src Kinase
J. Biol. Chem., January 31, 2003; 278(6): 3664 - 3670.
[Abstract] [Full Text] [PDF]


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