Skip to main content
Top
Published in: Gut Pathogens 1/2017

Open Access 01-12-2017 | Research

Helicobacter pylori vacA s1m1 genotype but not cagA or babA2 increase the risk of ulcer and gastric cancer in patients from Southern Mexico

Authors: Adolfo Román-Román, Dinorah Nashely Martínez-Carrillo, Josefina Atrisco-Morales, Julio César Azúcar-Heziquio, Abner Saúl Cuevas-Caballero, Carlos Alberto Castañón-Sánchez, Roxana Reyes-Ríos, Reyes Betancourt-Linares, Salomón Reyes-Navarrete, Iván Cruz-del Carmen, Margarita Camorlinga-Ponce, Enoc Mariano Cortés-Malagón, Gloria Fernández-Tilapa

Published in: Gut Pathogens | Issue 1/2017

Login to get access

Abstract

Background

The vacA, cagA and babA2 genotypes of Helicobacter pylori are associated with gastric pathology. The objectives were to determine the frequency of infection and distribution of the vacA, cagA and babA2 genotypes of H. pylori in patients with gastric ulcer, chronic gastritis and gastric cancer, and to evaluate the association of virulent genotypes with diagnosis.

Methods

We studied 921 patients with symptoms of dyspepsia or with presumptive diagnosis of gastric cancer. The DNA of H. pylori and the vacA, cagA and babA2 genes was detected by PCR in total DNA from gastric biopsies. The association of H. pylori and of its cagA, vacA and babA2 genotypes with diagnosis was determined by calculating the odds ratio (OR).

Results

Chronic gastritis was confirmed in 767 patients, gastric ulcer in 115 and cancer in 39. The prevalence of H. pylori was 47.8, 49.6 and 61.5% in those groups, respectively. H. pylori was more frequent in the surrounding tissue (69.2%) than in the tumor (53.8%). The vacA s1m1 genotype predominated in the three groups (45.2, 61.4 and 83.3%, respectively). H. pylori was associated with cancer (ORadjusted = 2.08; 95% CI 1.05–4.13; p = 0.035) but not with ulcer (ORadjusted = 1.07; 95% CI 0.71–1.61; p = 0.728). The s1m1 genotype was associated with ulcer and cancer (ORadjusted = 2.02; 95% CI 1.12–3.62; p = 0.019 and ORadjusted = 6.58; 95% CI 2.15–20.08; p = 0.001, respectively). babA2 was associated with gastric cancer, and cagA was not associated with the diagnosis.

Conclusions

In population from Southern Mexico, H. pylori and the s1m1 genotype were associated with gastric cancer and the s1m1/cagA+/babA2+ strains predominated in tumor and adjacent tissue.
Literature
1.
go back to reference Wroblewski LE, Peek RM Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev. 2010;23:713–39.CrossRefPubMedPubMedCentral Wroblewski LE, Peek RM Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev. 2010;23:713–39.CrossRefPubMedPubMedCentral
2.
go back to reference Ishijima N, Suzuki M, Ashida H, Ichikawa Y, Kanegae Y, Saito I, et al. BabA-mediated adherence is a potentiator of the Helicobacter pylori type IV secretion system activity. J Biol Chem. 2011;286(28):25256–64.CrossRefPubMedPubMedCentral Ishijima N, Suzuki M, Ashida H, Ichikawa Y, Kanegae Y, Saito I, et al. BabA-mediated adherence is a potentiator of the Helicobacter pylori type IV secretion system activity. J Biol Chem. 2011;286(28):25256–64.CrossRefPubMedPubMedCentral
3.
go back to reference Azevedo NF, Guimarães N, Figueiredo C, Keevil CW, Vieira MJ. New model for the transmission of Helicobacter pylori: role of environmental reservoirs as gene pools to increase train diversity. Crit Rev Microbiol. 2007;33:157–9.CrossRefPubMed Azevedo NF, Guimarães N, Figueiredo C, Keevil CW, Vieira MJ. New model for the transmission of Helicobacter pylori: role of environmental reservoirs as gene pools to increase train diversity. Crit Rev Microbiol. 2007;33:157–9.CrossRefPubMed
4.
go back to reference Sahara S, Sugimoto M, Vilaichone RK, Mahachai V, Miyajima H, Furuta T, et al. Role of Helicobacter pylori cagA EPIYA motif and vacA genotypes for the development of gastrointestinal diseases in Southeast Asian countries: a meta-analysis. BMC Infect Dis. 2012;12:223.CrossRefPubMedPubMedCentral Sahara S, Sugimoto M, Vilaichone RK, Mahachai V, Miyajima H, Furuta T, et al. Role of Helicobacter pylori cagA EPIYA motif and vacA genotypes for the development of gastrointestinal diseases in Southeast Asian countries: a meta-analysis. BMC Infect Dis. 2012;12:223.CrossRefPubMedPubMedCentral
5.
go back to reference Belkind-Gerson J, Basurto G. Incidencia de la infección por Helicobacter pylori en una cohorte de lactantes de Morelos. Salud Publ Mex. 2001;43:122–6. Belkind-Gerson J, Basurto G. Incidencia de la infección por Helicobacter pylori en una cohorte de lactantes de Morelos. Salud Publ Mex. 2001;43:122–6.
6.
go back to reference Martínez-Carrillo DN, Garza-Gonzalez E, Bertancourt-Linares R, Mónico-Manzano T, Antúnez-Rivera C, Román-Román A, et al. Association of IL1B-511C/-31T haplotype and Helicobacter pylori vacA genotypes with gastric ulcer and chronic gastritis. BMC Gastroenterol. 2010;10:126–32.CrossRefPubMedPubMedCentral Martínez-Carrillo DN, Garza-Gonzalez E, Bertancourt-Linares R, Mónico-Manzano T, Antúnez-Rivera C, Román-Román A, et al. Association of IL1B-511C/-31T haplotype and Helicobacter pylori vacA genotypes with gastric ulcer and chronic gastritis. BMC Gastroenterol. 2010;10:126–32.CrossRefPubMedPubMedCentral
7.
go back to reference Fernández-Tilapa G, Axinecuilteco-Hilera J, Giono-Cerezo S, Martínez-Carrillo DN, Illades-Aguiar B, Román-Román A. vacA genotypes in oral cavity and Helicobacter pylori seropositivity among adults without dyspepsia. Med Oral Pathol Oral Cir Buccal. 2011;16:e175–80.CrossRef Fernández-Tilapa G, Axinecuilteco-Hilera J, Giono-Cerezo S, Martínez-Carrillo DN, Illades-Aguiar B, Román-Román A. vacA genotypes in oral cavity and Helicobacter pylori seropositivity among adults without dyspepsia. Med Oral Pathol Oral Cir Buccal. 2011;16:e175–80.CrossRef
8.
go back to reference Cárdenas-Mondragón MG, Torres J, Flores-Luna L, Carreón-Talavera R, Camorlinga-Ponce M, Fuentes-Pananá EM. Epstein–Barr virus association with peptic ulcer disease. Anal Cell Pathol. 2015;2015:164840.CrossRef Cárdenas-Mondragón MG, Torres J, Flores-Luna L, Carreón-Talavera R, Camorlinga-Ponce M, Fuentes-Pananá EM. Epstein–Barr virus association with peptic ulcer disease. Anal Cell Pathol. 2015;2015:164840.CrossRef
9.
go back to reference Morales-Espinosa R, Fernandez-Presas A, Gonzalez-Valencia G, Flores-Hernandez S, Delgado-Sapien G, Mendez-Sanchez JL, et al. Helicobacter pylori in the oral cavity is associated with gastroesophageal disease. Oral Microbiol Immunol. 2009;24:464–8.CrossRefPubMed Morales-Espinosa R, Fernandez-Presas A, Gonzalez-Valencia G, Flores-Hernandez S, Delgado-Sapien G, Mendez-Sanchez JL, et al. Helicobacter pylori in the oral cavity is associated with gastroesophageal disease. Oral Microbiol Immunol. 2009;24:464–8.CrossRefPubMed
10.
go back to reference Paniagua GL, Monroy E, Rodríguez R, Arroniz S, Rodríguez C, Cortés JL, et al. Frequency of vacA, cagA and babA2 virulence markers in Helicobacter pylori strains isolated from Mexican patients with chronic gastritis. Ann Clin Microbiol Antimicrob. 2009;8:14.CrossRefPubMedPubMedCentral Paniagua GL, Monroy E, Rodríguez R, Arroniz S, Rodríguez C, Cortés JL, et al. Frequency of vacA, cagA and babA2 virulence markers in Helicobacter pylori strains isolated from Mexican patients with chronic gastritis. Ann Clin Microbiol Antimicrob. 2009;8:14.CrossRefPubMedPubMedCentral
11.
go back to reference Román-Román A, Giono-Cerezo S, Camorlinga-Ponce M, Martínez-Carrillo DN, Loaiza-Loeza S, Fernández-Tilapa G. vacA genotypes of Helicobacter pylori in the oral cavity and stomach of patients with chronic gastritis and gastric ulcer. Enferm Infecc Microbiol Clin. 2013;31(3):130–5.CrossRefPubMed Román-Román A, Giono-Cerezo S, Camorlinga-Ponce M, Martínez-Carrillo DN, Loaiza-Loeza S, Fernández-Tilapa G. vacA genotypes of Helicobacter pylori in the oral cavity and stomach of patients with chronic gastritis and gastric ulcer. Enferm Infecc Microbiol Clin. 2013;31(3):130–5.CrossRefPubMed
12.
go back to reference Cárdenas-Mondragón MG, Torres J, Flores-Luna L, Camorlinga-Ponce M, Carreón-Talavera R, Gomez-Delgado A, et al. Case-control study of Epstein–Barr virus and Helicobacter pylori serology in Latin American patients with gastric disease. Br J Cancer. 2015;112(12):1866–73.CrossRefPubMedPubMedCentral Cárdenas-Mondragón MG, Torres J, Flores-Luna L, Camorlinga-Ponce M, Carreón-Talavera R, Gomez-Delgado A, et al. Case-control study of Epstein–Barr virus and Helicobacter pylori serology in Latin American patients with gastric disease. Br J Cancer. 2015;112(12):1866–73.CrossRefPubMedPubMedCentral
13.
go back to reference Con SA, Takeuchi H, Con-Chin GR, Con-Chin VG, Yasuda N, Con-Wong R. Role of bacterial and genetic factors in gastric cancer in Costa Rica. World J Gastroenterol. 2009;15(2):211–8.CrossRefPubMedPubMedCentral Con SA, Takeuchi H, Con-Chin GR, Con-Chin VG, Yasuda N, Con-Wong R. Role of bacterial and genetic factors in gastric cancer in Costa Rica. World J Gastroenterol. 2009;15(2):211–8.CrossRefPubMedPubMedCentral
14.
go back to reference Latifi-Navid S, Mohammadi S, Maleki P, Zahri S, Yazdanbod A, Siavoshi F, et al. Helicobacter pylori vacA d1/-i1 genotypes and geographic differentiation between high and low incidence areas of gastric cancer in Iran. Arch Iran Med. 2013;16(6):330–7.PubMed Latifi-Navid S, Mohammadi S, Maleki P, Zahri S, Yazdanbod A, Siavoshi F, et al. Helicobacter pylori vacA d1/-i1 genotypes and geographic differentiation between high and low incidence areas of gastric cancer in Iran. Arch Iran Med. 2013;16(6):330–7.PubMed
15.
go back to reference Arévalo-Galvis A, Trespalacios-Rangel AA, Otero W, Mercado-Reyes MM, Poutou-Piñales RA. Prevalence of cagA, vacA, and iceA genes in H. pylori strains isolated from Colombian patients with functional dispepsia. Pol J Microbiol. 2012;61(1):33–40.PubMed Arévalo-Galvis A, Trespalacios-Rangel AA, Otero W, Mercado-Reyes MM, Poutou-Piñales RA. Prevalence of cagA, vacA, and iceA genes in H. pylori strains isolated from Colombian patients with functional dispepsia. Pol J Microbiol. 2012;61(1):33–40.PubMed
16.
go back to reference Gerhard M, Lehn N, Neumayer N, Borén T, Rad R, Schepp W, et al. Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin. Proc Natl Acad Sci USA. 1999;96:12778–83.CrossRefPubMedPubMedCentral Gerhard M, Lehn N, Neumayer N, Borén T, Rad R, Schepp W, et al. Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin. Proc Natl Acad Sci USA. 1999;96:12778–83.CrossRefPubMedPubMedCentral
17.
go back to reference Acevedo M, Eriksson S, Mendes N, Serpa J, Figueiredo C, Resende LP, et al. Infection by Helicobacter pylori expressing the BabA adhesin is influenced by the secretor phenotype. J Pathol. 2008;215(3):308–16.CrossRef Acevedo M, Eriksson S, Mendes N, Serpa J, Figueiredo C, Resende LP, et al. Infection by Helicobacter pylori expressing the BabA adhesin is influenced by the secretor phenotype. J Pathol. 2008;215(3):308–16.CrossRef
18.
go back to reference Chomvarin C, Namwat W, Chaicumpar K, Mairiang P, Sangchan A, Sripa B, et al. Prevalence of Helicobacter pylori vacA, cagA, cagE, iceA and babA2 genotypes in Thai dyspeptic patients. Int J Infect Dis. 2008;12(1):30–6.CrossRefPubMed Chomvarin C, Namwat W, Chaicumpar K, Mairiang P, Sangchan A, Sripa B, et al. Prevalence of Helicobacter pylori vacA, cagA, cagE, iceA and babA2 genotypes in Thai dyspeptic patients. Int J Infect Dis. 2008;12(1):30–6.CrossRefPubMed
19.
go back to reference Torres LE, Melián K, Moreno A, Alonso J, Sabatier CA, Hernández M, et al. Prevalence of vacA, cagA and babA2 genes in Cuban Helicobacter pylori isolates. World J Gastroenterol. 2009;15(2):204–10.CrossRefPubMedPubMedCentral Torres LE, Melián K, Moreno A, Alonso J, Sabatier CA, Hernández M, et al. Prevalence of vacA, cagA and babA2 genes in Cuban Helicobacter pylori isolates. World J Gastroenterol. 2009;15(2):204–10.CrossRefPubMedPubMedCentral
20.
go back to reference Oliveira AG, Santos A, Guerra JB, Rocha GA, Rocha AM, Oliveira CA, et al. babA2- and cagA-positive Helicobacter pylori strains are associated with duodenal ulcer and gastric carcinoma in Brazil. J Clin Microbiol. 2003;41(8):3964–6.CrossRefPubMedPubMedCentral Oliveira AG, Santos A, Guerra JB, Rocha GA, Rocha AM, Oliveira CA, et al. babA2- and cagA-positive Helicobacter pylori strains are associated with duodenal ulcer and gastric carcinoma in Brazil. J Clin Microbiol. 2003;41(8):3964–6.CrossRefPubMedPubMedCentral
21.
go back to reference Sgouras DN, Panayotopoulou EG, Papadakos K, Martinez-Gonzalez B, Roumbani A, Panayiotou J, et al. CagA and VacA polymorphisms do not correlate with severity of histopathological lesions in Helicobacter pylori-infected Greek children. J Clin Microbiol. 2009;47(8):2426–34.CrossRefPubMedPubMedCentral Sgouras DN, Panayotopoulou EG, Papadakos K, Martinez-Gonzalez B, Roumbani A, Panayiotou J, et al. CagA and VacA polymorphisms do not correlate with severity of histopathological lesions in Helicobacter pylori-infected Greek children. J Clin Microbiol. 2009;47(8):2426–34.CrossRefPubMedPubMedCentral
22.
go back to reference Acosta N, Quiroga A, Delgado P, Mercedes B, Jaramillo C. Helicobacter pylori CagA protein polymorphisms and their lack of association with pathogenesis. World J Gastroenterol. 2010;16(31):3936–43.CrossRefPubMedPubMedCentral Acosta N, Quiroga A, Delgado P, Mercedes B, Jaramillo C. Helicobacter pylori CagA protein polymorphisms and their lack of association with pathogenesis. World J Gastroenterol. 2010;16(31):3936–43.CrossRefPubMedPubMedCentral
23.
go back to reference Woon AP, Tohidpour A, Alonso H, Saijo-Hamano Y, Kwok T, Roujeinikova A. Conformational analysis of isolated domains of Helicobacter pylori CagA. PLoS ONE. 2013;8(11):e7936.CrossRef Woon AP, Tohidpour A, Alonso H, Saijo-Hamano Y, Kwok T, Roujeinikova A. Conformational analysis of isolated domains of Helicobacter pylori CagA. PLoS ONE. 2013;8(11):e7936.CrossRef
24.
go back to reference Nogueira C, Figueiredo C, Carneiro F, Gomes AT, Barreira R, Figueira P, et al. Helicobacter pylori genotypes may determine gastric histopathology. Am J Parasitol. 2001;158:647–54. Nogueira C, Figueiredo C, Carneiro F, Gomes AT, Barreira R, Figueira P, et al. Helicobacter pylori genotypes may determine gastric histopathology. Am J Parasitol. 2001;158:647–54.
25.
go back to reference Matteo MJ, Granados G, Peréz CV, Olmos M, Sanchez C, Catalano M. Helicobacter pylori cagA pathogenicity island genotype diversity the gastric niche of a single host. J Med Microbiol. 2007;56:664–9.CrossRefPubMed Matteo MJ, Granados G, Peréz CV, Olmos M, Sanchez C, Catalano M. Helicobacter pylori cagA pathogenicity island genotype diversity the gastric niche of a single host. J Med Microbiol. 2007;56:664–9.CrossRefPubMed
26.
go back to reference Nomura AM, Pérez-Pérez GI, Lee J, Stemmermann G, Blaser MJ. Relation between Helicobacter pylori cagA status and risk of peptic ulcer disease. Am J Epidemiol. 2002;155(11):1054–9.CrossRefPubMed Nomura AM, Pérez-Pérez GI, Lee J, Stemmermann G, Blaser MJ. Relation between Helicobacter pylori cagA status and risk of peptic ulcer disease. Am J Epidemiol. 2002;155(11):1054–9.CrossRefPubMed
27.
go back to reference Torres J, Lopez L, Lazcano E, Camorlinga M, Flores L, Muñoz O. Trends in Helicobacter pylori infection and gastric cancer in Mexico. Cancer Epidemiol Biomark Prev. 2005;14:1874–7.CrossRef Torres J, Lopez L, Lazcano E, Camorlinga M, Flores L, Muñoz O. Trends in Helicobacter pylori infection and gastric cancer in Mexico. Cancer Epidemiol Biomark Prev. 2005;14:1874–7.CrossRef
28.
go back to reference Murata-Kamiya N. Pathophysiological functions of the CagA oncoprotein during infection by Helicobacter pylori. Microbes Infect. 2011;13:799–807.CrossRefPubMed Murata-Kamiya N. Pathophysiological functions of the CagA oncoprotein during infection by Helicobacter pylori. Microbes Infect. 2011;13:799–807.CrossRefPubMed
29.
30.
go back to reference Miernyk K, Morris J, Bruden D, McMahon B, Hurlburt D, Sacco F, et al. Characterization of Helicobacter pylori cagA and vacA genotypes among Alaskans and their correlation with clinical disease. J Clin Microbiol. 2011;49(9):3114–21.CrossRefPubMedPubMedCentral Miernyk K, Morris J, Bruden D, McMahon B, Hurlburt D, Sacco F, et al. Characterization of Helicobacter pylori cagA and vacA genotypes among Alaskans and their correlation with clinical disease. J Clin Microbiol. 2011;49(9):3114–21.CrossRefPubMedPubMedCentral
31.
go back to reference Rudi J, Kolb C, Maiwald M, Kuck D, Sieg A, Galle PR, et al. Diversity of Helicobacter pylori vacA and cagA genes and relationship to VacA and CagA protein expression, cytotoxin production, and associated diseases. J Clin Microbiol. 1998;36(4):944–8.PubMedPubMedCentral Rudi J, Kolb C, Maiwald M, Kuck D, Sieg A, Galle PR, et al. Diversity of Helicobacter pylori vacA and cagA genes and relationship to VacA and CagA protein expression, cytotoxin production, and associated diseases. J Clin Microbiol. 1998;36(4):944–8.PubMedPubMedCentral
32.
go back to reference Gangwer KA, Shaffer CL, Suerbaum S, Lacy DB, Cover TL, Bordenstein SR. Molecular evolution of the Helicobacter pylori vacuolating toxin gene vacA. J Bacteriol. 2010;192(23):6126–35.CrossRefPubMedPubMedCentral Gangwer KA, Shaffer CL, Suerbaum S, Lacy DB, Cover TL, Bordenstein SR. Molecular evolution of the Helicobacter pylori vacuolating toxin gene vacA. J Bacteriol. 2010;192(23):6126–35.CrossRefPubMedPubMedCentral
33.
go back to reference Marciorkowska E, Roszko I, Kowalczuk O, Kaczmarski M, Chyczewski L, Kemona A. The evaluation of vacA gene alleles frequency in Helicobacter pylori strains in adults in Podlaskies children and region. Folia Histochem Cytobiol. 2007;45(3):215–9. Marciorkowska E, Roszko I, Kowalczuk O, Kaczmarski M, Chyczewski L, Kemona A. The evaluation of vacA gene alleles frequency in Helicobacter pylori strains in adults in Podlaskies children and region. Folia Histochem Cytobiol. 2007;45(3):215–9.
34.
go back to reference Martins LC, Corvelo TC, Demachki S, Araujo MT, Assumpҫão MB, Vilar SC, et al. Clinical and pathological importance of vacA allele heterogeneity and cagA status in peptic ulcer disease in patients from North Brazil. Mem Inst Oswaldo Cruz. 2005;100(8):875–81.CrossRefPubMed Martins LC, Corvelo TC, Demachki S, Araujo MT, Assumpҫão MB, Vilar SC, et al. Clinical and pathological importance of vacA allele heterogeneity and cagA status in peptic ulcer disease in patients from North Brazil. Mem Inst Oswaldo Cruz. 2005;100(8):875–81.CrossRefPubMed
35.
go back to reference Atherton JC, Cao P, Peek RM, Tummuru MKR, Blasser MJ, Cover TL. Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. J Biol Chem. 1995;270:17771–7.CrossRefPubMed Atherton JC, Cao P, Peek RM, Tummuru MKR, Blasser MJ, Cover TL. Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. J Biol Chem. 1995;270:17771–7.CrossRefPubMed
37.
go back to reference Chang YH, Wang L, Lee MS, Cheng CW, Wu CY, Shiau MY. Genotypic characterization of Helicobacter pylori cagA and vacA from biopsy specimens of patients with gastroduodenal diseases. Mt Sinai J Med. 2006;73:622–6.PubMed Chang YH, Wang L, Lee MS, Cheng CW, Wu CY, Shiau MY. Genotypic characterization of Helicobacter pylori cagA and vacA from biopsy specimens of patients with gastroduodenal diseases. Mt Sinai J Med. 2006;73:622–6.PubMed
39.
go back to reference Secretaría de Salud de México. Sistema Nacional de Vigilancia Epidemiológica. Sistema Único de Información. Panorama epidemiológico de las úlceras, gastritis y duodenitis en México, periodo 2003–2008 (primera de dos partes). Boletín de Epidemiología. 2010;27(18):1–47. Secretaría de Salud de México. Sistema Nacional de Vigilancia Epidemiológica. Sistema Único de Información. Panorama epidemiológico de las úlceras, gastritis y duodenitis en México, periodo 2003–2008 (primera de dos partes). Boletín de Epidemiología. 2010;27(18):1–47.
40.
go back to reference Abdo-Francis JM, Uscanga L, Sobrino-Cossio S, Rivera-Ramos JF, Huerta-Iga F, Tamayo de la Cuesta JL. Consenso Mexicano sobre Helicobacter pylori. Rev Gastroenterol Mex. 2007;72(3):323–38.PubMed Abdo-Francis JM, Uscanga L, Sobrino-Cossio S, Rivera-Ramos JF, Huerta-Iga F, Tamayo de la Cuesta JL. Consenso Mexicano sobre Helicobacter pylori. Rev Gastroenterol Mex. 2007;72(3):323–38.PubMed
41.
go back to reference World Health Organization. International Agency for Research on Cancer. Globocan 2012: estimated cancer incidence, mortality and prevalence worldwide 2012. http://globocan.iarc.fr/. Accessed 06 Oct 2016. World Health Organization. International Agency for Research on Cancer. Globocan 2012: estimated cancer incidence, mortality and prevalence worldwide 2012. http://​globocan.​iarc.​fr/​. Accessed 06 Oct 2016.
42.
go back to reference Morales-Espinoza R, Castillo-Rojas G, Gonzalez-Valencia G, Ponce-de-León S, Cravioto A, Atherton CJ, et al. Colonization of Mexican patients by multiple Helicobacter pylori strains with different vacA and cagA genotypes. J Clin Microbiol. 1999;37:3001–4. Morales-Espinoza R, Castillo-Rojas G, Gonzalez-Valencia G, Ponce-de-León S, Cravioto A, Atherton CJ, et al. Colonization of Mexican patients by multiple Helicobacter pylori strains with different vacA and cagA genotypes. J Clin Microbiol. 1999;37:3001–4.
43.
go back to reference Garza-González E, Bosques-Padilla FJ, Tijerina-Menchaca R, Pérez-Pérez GI. Characterization of Helicobacter pylori isolates from the north-eastern region of Mexico. Clin Microbiol Infect. 2004;10:41–5.CrossRefPubMed Garza-González E, Bosques-Padilla FJ, Tijerina-Menchaca R, Pérez-Pérez GI. Characterization of Helicobacter pylori isolates from the north-eastern region of Mexico. Clin Microbiol Infect. 2004;10:41–5.CrossRefPubMed
44.
go back to reference López-Vidal Y, Ponce-de-León S, Castillo-Rojas G, Barreto-Zuñiga R, Torre-Delgadillo A. High diversity of vacA and cagA Helicobacter pylori genotypes in patients with and without gastric cancer. PLoS ONE. 2008;3(12):e3849.CrossRefPubMedPubMedCentral López-Vidal Y, Ponce-de-León S, Castillo-Rojas G, Barreto-Zuñiga R, Torre-Delgadillo A. High diversity of vacA and cagA Helicobacter pylori genotypes in patients with and without gastric cancer. PLoS ONE. 2008;3(12):e3849.CrossRefPubMedPubMedCentral
45.
go back to reference González-Valencia G, Atherton JC, Muñoz O, Dehesa M, la Garza AM, Torres J. Helicobacter pylori vacA and cagA genotypes in Mexican adults and children. J Infect Dis. 2000;182(5):1450–4.CrossRefPubMed González-Valencia G, Atherton JC, Muñoz O, Dehesa M, la Garza AM, Torres J. Helicobacter pylori vacA and cagA genotypes in Mexican adults and children. J Infect Dis. 2000;182(5):1450–4.CrossRefPubMed
46.
go back to reference Stolte M, Meining A. The updated Sydney system: classification and grading of gastritis as the basis of diagnosis and treatment. Can J Gastroenterol. 2001;15(9):591–8.CrossRefPubMed Stolte M, Meining A. The updated Sydney system: classification and grading of gastritis as the basis of diagnosis and treatment. Can J Gastroenterol. 2001;15(9):591–8.CrossRefPubMed
47.
go back to reference Rugge M, Correa P, Dixon MF, Hattori T, Leandro G, Lewin K, et al. Gastric dysplasia: the Padova international classification. Am J Surg Pathol. 2000;24(2):167–76.CrossRefPubMed Rugge M, Correa P, Dixon MF, Hattori T, Leandro G, Lewin K, et al. Gastric dysplasia: the Padova international classification. Am J Surg Pathol. 2000;24(2):167–76.CrossRefPubMed
48.
go back to reference Sambrook J, Russel D. Molecular cloning a laboratory manual. New York: Cold Spring Harbor Laboratory Press; 2001. Sambrook J, Russel D. Molecular cloning a laboratory manual. New York: Cold Spring Harbor Laboratory Press; 2001.
49.
go back to reference Park CY, Kwak M, Gutierrez O, et al. Comparison of genotyping Helicobacter pylori directly from biopsy specimens and genotyping from bacterial cultures. J Clin Microbiol. 2003;41:3336–8.CrossRefPubMedPubMedCentral Park CY, Kwak M, Gutierrez O, et al. Comparison of genotyping Helicobacter pylori directly from biopsy specimens and genotyping from bacterial cultures. J Clin Microbiol. 2003;41:3336–8.CrossRefPubMedPubMedCentral
50.
go back to reference Figura N, Vindigni C, Covacci A, Presenti L, Burroni D, Vernillo R, et al. cagA positive and negative Helicobacter pylori strains are simultaneously present in the stomach of most patients with non-ulcer dyspepsia: relevance to histological damage. Gut. 1998;42(6):772–8.CrossRefPubMedPubMedCentral Figura N, Vindigni C, Covacci A, Presenti L, Burroni D, Vernillo R, et al. cagA positive and negative Helicobacter pylori strains are simultaneously present in the stomach of most patients with non-ulcer dyspepsia: relevance to histological damage. Gut. 1998;42(6):772–8.CrossRefPubMedPubMedCentral
51.
go back to reference Argent RH, Zhang Y, Atherton JC. Simple method for determination of the number of Helicobacter pylori CagA variable-region EPIYA tyrosine phosphorylation motifs by PCR. J Clin Microbiol. 2005;43:791–5.CrossRefPubMedPubMedCentral Argent RH, Zhang Y, Atherton JC. Simple method for determination of the number of Helicobacter pylori CagA variable-region EPIYA tyrosine phosphorylation motifs by PCR. J Clin Microbiol. 2005;43:791–5.CrossRefPubMedPubMedCentral
52.
go back to reference Salih BA, Bolek BK, Arikan S. DNA sequence analysis of cagA 3′ motifs of Helicobacter pylori strains from patients with peptic ulcer diseases. J Med Microbiol. 2010;59(Pt 2):144–8.CrossRefPubMed Salih BA, Bolek BK, Arikan S. DNA sequence analysis of cagA 3′ motifs of Helicobacter pylori strains from patients with peptic ulcer diseases. J Med Microbiol. 2010;59(Pt 2):144–8.CrossRefPubMed
54.
go back to reference Tang YL, Gan RL, Dong BH, Jiang RC, Tang RJ. Detection and location of Helicobacter pylori in human gastric carcinomas. World J Gastroenterol. 2005;11(9):1387–91.CrossRefPubMedPubMedCentral Tang YL, Gan RL, Dong BH, Jiang RC, Tang RJ. Detection and location of Helicobacter pylori in human gastric carcinomas. World J Gastroenterol. 2005;11(9):1387–91.CrossRefPubMedPubMedCentral
55.
go back to reference Zhang C, Yamada N, Wu YL, Wen M, Matsuhisa T, Matsukura N. Comparison of Helicobacter pylori infection and gastric mucosal histological features of gastric ulcer patients with chronic gastritis patients. World J Gastroenterol. 2005;11(7):976–81.CrossRefPubMedPubMedCentral Zhang C, Yamada N, Wu YL, Wen M, Matsuhisa T, Matsukura N. Comparison of Helicobacter pylori infection and gastric mucosal histological features of gastric ulcer patients with chronic gastritis patients. World J Gastroenterol. 2005;11(7):976–81.CrossRefPubMedPubMedCentral
56.
go back to reference Inoue K, Shiota S, Yamada K, Gotoh K, Suganuma M, Fujioka T, et al. Evaluation of a new tumor necrosis factor-α-inducing membrane protein of Helicobacter pylori as a prophylactic vaccine antigen. Helicobacter. 2009;14:135–43.CrossRefPubMed Inoue K, Shiota S, Yamada K, Gotoh K, Suganuma M, Fujioka T, et al. Evaluation of a new tumor necrosis factor-α-inducing membrane protein of Helicobacter pylori as a prophylactic vaccine antigen. Helicobacter. 2009;14:135–43.CrossRefPubMed
57.
go back to reference Wang J, Chi DS, Laffan JJ, Li C, Ferguson DA, Litchfield P, et al. Comparison of cytotoxin genotypes of Helicobacter pylori in stomach and saliva. Dig Dis Sci. 2002;47(8):1850–6.CrossRefPubMed Wang J, Chi DS, Laffan JJ, Li C, Ferguson DA, Litchfield P, et al. Comparison of cytotoxin genotypes of Helicobacter pylori in stomach and saliva. Dig Dis Sci. 2002;47(8):1850–6.CrossRefPubMed
58.
go back to reference Assumpção MB, Martins LC, Melo Barbosa HP, Barile KA, de Almeida SS, Assumpcão PP, et al. Helicobacter pylori in dental plaque and stomach of patients from Northern Brazil. World J Gastroenterol. 2010;16(24):3033–9.CrossRefPubMedPubMedCentral Assumpção MB, Martins LC, Melo Barbosa HP, Barile KA, de Almeida SS, Assumpcão PP, et al. Helicobacter pylori in dental plaque and stomach of patients from Northern Brazil. World J Gastroenterol. 2010;16(24):3033–9.CrossRefPubMedPubMedCentral
59.
go back to reference Smith JG, Kong L, Abruzzo GK, Gill CJ, Flattery AM, Scott PM, et al. PCR detection of colonization by Helicobacter pylori in conventional, euthymic mice based on the 16S ribosomal gene sequence. Clin Diagn Lab Immunol. 1996;3(1):66–72.PubMedPubMedCentral Smith JG, Kong L, Abruzzo GK, Gill CJ, Flattery AM, Scott PM, et al. PCR detection of colonization by Helicobacter pylori in conventional, euthymic mice based on the 16S ribosomal gene sequence. Clin Diagn Lab Immunol. 1996;3(1):66–72.PubMedPubMedCentral
60.
go back to reference Silva MR, Vinagre RM, Silva AV, Oliveira CS, Santos KN, Costa RA, et al. Differences in virulence markers between Helicobacter pylori strains from the Brazilian Amazon región. Rev Soc Bras Med Trop. 2013;46(3):358–61.CrossRefPubMed Silva MR, Vinagre RM, Silva AV, Oliveira CS, Santos KN, Costa RA, et al. Differences in virulence markers between Helicobacter pylori strains from the Brazilian Amazon región. Rev Soc Bras Med Trop. 2013;46(3):358–61.CrossRefPubMed
61.
go back to reference Figueiredo C, Van Doorn LJ, Nogueira C, Soares JM, Pinho C, Figueira P, et al. Helicobacter pylori genotypes are associated with clinical outcome in Portuguese patients and show a high prevalence of infections with multiple strains. Scand J Gastroenterol. 2001;36(2):128–35.CrossRefPubMed Figueiredo C, Van Doorn LJ, Nogueira C, Soares JM, Pinho C, Figueira P, et al. Helicobacter pylori genotypes are associated with clinical outcome in Portuguese patients and show a high prevalence of infections with multiple strains. Scand J Gastroenterol. 2001;36(2):128–35.CrossRefPubMed
62.
go back to reference Blaser MJ, Perez-Perez GI, Kleanthous H, Cover TL, Peek RM, Chyou PH, et al. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res. 1995;55(10):2111–5.PubMed Blaser MJ, Perez-Perez GI, Kleanthous H, Cover TL, Peek RM, Chyou PH, et al. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res. 1995;55(10):2111–5.PubMed
63.
go back to reference Kuipers EJ, Perez-Perez GI, Meuwissen SG, Blaser MJ. Helicobacter pylori and atrophic gastritis. Importance of the cagA status. J Natl Cancer Inst. 1995;87(23):1777–80.CrossRefPubMed Kuipers EJ, Perez-Perez GI, Meuwissen SG, Blaser MJ. Helicobacter pylori and atrophic gastritis. Importance of the cagA status. J Natl Cancer Inst. 1995;87(23):1777–80.CrossRefPubMed
64.
go back to reference Wang SK, Zhu HF, He BS, Zhang ZY, Chen ZT, Wang ZZ, et al. CagA+ H. pylori infection is associated with polarization of T helper cell immune responses in gastric carcinogenesis. World J Gastroenterol. 2007;13(21):2923–31.CrossRefPubMedPubMedCentral Wang SK, Zhu HF, He BS, Zhang ZY, Chen ZT, Wang ZZ, et al. CagA+ H. pylori infection is associated with polarization of T helper cell immune responses in gastric carcinogenesis. World J Gastroenterol. 2007;13(21):2923–31.CrossRefPubMedPubMedCentral
65.
go back to reference Wang F, Meng W, Wang B, Qiao L. Helicobacter pylori-induce gastric inflammation and gastric cancer. Cancer Lett. 2014;345(2):196–202.CrossRefPubMed Wang F, Meng W, Wang B, Qiao L. Helicobacter pylori-induce gastric inflammation and gastric cancer. Cancer Lett. 2014;345(2):196–202.CrossRefPubMed
66.
go back to reference Yu H, Zeng J, Liang X, Wang W, Zhou Y, Sun Y, et al. Helicobacter pylori promotes epithelial–mesenchymal transition in gastric cancer by downregulating programmed cell death protein 4 (PDCD4). PLoS ONE. 2014;9(8):e105306.CrossRefPubMedPubMedCentral Yu H, Zeng J, Liang X, Wang W, Zhou Y, Sun Y, et al. Helicobacter pylori promotes epithelial–mesenchymal transition in gastric cancer by downregulating programmed cell death protein 4 (PDCD4). PLoS ONE. 2014;9(8):e105306.CrossRefPubMedPubMedCentral
67.
go back to reference Yamaoka Y, Souchek J, Odenbreit S, Haas R, Arngvist A, Borén T, et al. Discrimination between cases of duodenal ulcer and gastritis on the basis of putative virulence factors of Helicobacter pylori. J Clin Microbiol. 2002;40(6):2244–6.CrossRefPubMedPubMedCentral Yamaoka Y, Souchek J, Odenbreit S, Haas R, Arngvist A, Borén T, et al. Discrimination between cases of duodenal ulcer and gastritis on the basis of putative virulence factors of Helicobacter pylori. J Clin Microbiol. 2002;40(6):2244–6.CrossRefPubMedPubMedCentral
68.
go back to reference Gatti LL, Módena JL, Payão SL, MdeA Smith, Fukuhara Y, Módena JL, et al. Prevalence of Helicobacter pylori cagA, iceA and babA2 alleles in Brazilian patients with upper gastrointestinal diseases. Acta Trop. 2006;100:232–40.CrossRefPubMed Gatti LL, Módena JL, Payão SL, MdeA Smith, Fukuhara Y, Módena JL, et al. Prevalence of Helicobacter pylori cagA, iceA and babA2 alleles in Brazilian patients with upper gastrointestinal diseases. Acta Trop. 2006;100:232–40.CrossRefPubMed
69.
go back to reference Chen MY, He CY, Meng X, Yuan Y. Association of Helicobacter pylori babA2 with peptic ulcer disease and gastric cancer. World J Gastroenterol. 2013;19(26):4242–51.CrossRefPubMedPubMedCentral Chen MY, He CY, Meng X, Yuan Y. Association of Helicobacter pylori babA2 with peptic ulcer disease and gastric cancer. World J Gastroenterol. 2013;19(26):4242–51.CrossRefPubMedPubMedCentral
Metadata
Title
Helicobacter pylori vacA s1m1 genotype but not cagA or babA2 increase the risk of ulcer and gastric cancer in patients from Southern Mexico
Authors
Adolfo Román-Román
Dinorah Nashely Martínez-Carrillo
Josefina Atrisco-Morales
Julio César Azúcar-Heziquio
Abner Saúl Cuevas-Caballero
Carlos Alberto Castañón-Sánchez
Roxana Reyes-Ríos
Reyes Betancourt-Linares
Salomón Reyes-Navarrete
Iván Cruz-del Carmen
Margarita Camorlinga-Ponce
Enoc Mariano Cortés-Malagón
Gloria Fernández-Tilapa
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2017
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-017-0167-z

Other articles of this Issue 1/2017

Gut Pathogens 1/2017 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.