Original Research Open Access
Copyright ©The Author(s) 2001. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Aug 15, 2001; 7(4): 506-509
Published online Aug 15, 2001. doi: 10.3748/wjg.v7.i4.506
Glutathione S-transferases M1, T1 genotypes and the risk of gastric cancer: A case-control study
Lin Cai, Department of Epidemiology, Fujian Medical University, Fuzhou 350004, Fujian Province, China
Shun-Zhang Yu, Department of Epidemiology, Shanghai Medical University, Shanghai 200032, China
Zuo-Feng Zhang, Department of Epidemiology, UCLA School of Public Health, Los Angeles California, USA
Author contributions: All authors contributed equally to the work.
Supported by Natural Science Foundation of Fujian Province, China, No. C001009
Correspondence to: Lin Cai, Department of Epidemiology, Fujian Medical University, Fuzhou 350004, Fujian Province, China. zjcailin@pub5.fz.fj.cn
Telephone: 0086-591-3569264
Received: March 19, 2001
Revised: April 5, 2001
Accepted: April 12, 2001
Published online: August 15, 2001


AIM: Glutathione S-transferases (GSTs) are involved in the detoxification of many potential carcinogens and appear to play a critical role in the protection from the effects of carcinogens. The contribution of glutathione S-transferases M1 and T1 genotypes to susceptibility to the risk of gastric cancer and their interaction with cigarette smoking are still unclear. The aim of this study was to determine whether there was any relationship between genetic polymorphisms of GSTM1 and GSTT1 and gastric cancer.

METHODS: A population based case-control study was carried out in a high-risk area, Changle County, Fujian Province, China. The epidemiological data were collected by a standard questionnaire and blood samples were obtained from 95 incidence gastric cancer cases and 94 healthy controls. A polymerase chain reaction method was used to detect the presence or absence of the GSTM1 and GSTT1 genes in genomic DNA. Logistic regression model was employed in the data analysis.

RESULTS: An increase in risk for gastric cancer was found among carriers of GSTM1 null genotype. The adjusted odds ratio (OR) was 2.63 [95% Confidence Interval (95%CI) 1.17-5.88], after controlling for age, gender, cigarette smoking, alcohol drinking, and fish sauce intake. The frequency of GSTT1 null genotype in cancer cases (43.16%) was not significantly different from that in controls (50.00%). However, the risk for gastric cancer in those with GSTM1 null and GSTT1 non-null genotype was significantly higher than in those with both GSTM1 and GSTT1 non-null genotype (OR = 2.77, 95%CI 1.15-6.77). Compared with those subjects who never smoked and had normal GSTM1 genotype, ORs were 1.60 (95%CI: 0.62-4.19) for never smokers with GSTM1 null type, 2.33 (95%CI 0.88-6.28) for smokers with normal GSTM1, and 8.06 (95%CI 2.83-23.67) for smokers with GSTM1 null type.

CONCLUSIONS: GSTM1 gene polymorphisms may be associated with genetic susceptibility of stomach cancer and may modulate tobacco-related carcinogenesis of gastric cancer.

Key Words: glutathione transferase/genetics, genotype, polymorphism (genetics), stomach neoplasm/genetics, case control studies


Glutathione S-transferases (GSTs), a supergene family of detoxification enzymes, appear to form a protection mechanism against chemical carcinogenesis. In human tissues this family consists of four multigene classes, referred to as alpha, mu, pi, and theta. The GSTM1 gene is classified into the mu class and the GSTT1 gene belongs to the theta class. They detoxify reactive chemical species, such as polycyclic aromatic hydrocarbon epoxides by catalyzing their conjugation to glutathione. Genes coding for GSTM1 and GSTT1 proteins are polymorphic in humans and these genes are absent in 10%-60% of different ethnic populations[1,2]. Accumulating evidence indicates that susceptibility to cancer is mediated by genetically determined differences in the effectiveness of detoxification of potential carcinogens. Genetic differences are likely to be a major source of interindividual variation in susceptibility to cancer[3].

Gastric cancer is the most common cancer in whole China[4-8], especially in Changle County, Fujian Province, China[9,10]. Previous studies have shown that a number of environmental risk factors may play a role in a multistep and multifactorial process[11-13]. Tobacco smoking has been considered a potential risk factor for gastric cancer[14]. Few data have so far been reported on the risk of gastric cancer associated with genetic and environmental exposures. To evaluate the relationships between GSTM1/GSTT1 and gastric cancer, a molecular epidemiological study was conducted in Changle County.

Study subjects

Cases and controls were all residents in Changle County, China, which is one of areas with the highest rates of gastric cancer in the world. All primary gastric cancers (n = 95) were histologically confirmed or diagnosed by operation between January 1996 to March 1998. Population controls (n = 94) were randomly selected from the same geographical region, and matched to cases by their gender and age. The field staff conducted face-to-face interviews. Cases and controls were interviewed in the same manner using a standard epidemiological questionnaire. Blood samples (5 mL) were collected.

GSTM1 and GSTT1 Assay

DNA was isolated from peripheral white blood cells by proteinase K (Huamei Biotechnology, Inc.) digestion and phenol/chloroform extractions. The PCR reactions were performed in 50 μL of a solution containing PCR buffer (1.5 mmol·L-1 MgCl2, 50 mmol·L-1 KCl, 10 mmol·L-1 Tris-HCl, pH8.3), 200 μmol·L-1 of each dNTP, 1 μmol·L-1 of each primer, 200 ng of template DNA, and 2.5 unit of TAQ DNA polymerase (Promega). Primer sequences for GSTM1 were 5’-GCTTCACGTGTTATGGAGGTTC-3’ and 5’-GAGATGAAGTCCTCCAGATTT-3’, which produced a 157 base pair band. The GSTT1 primers were 5’-TTCCTTACTGGTCCTCACATCTC-3’ and 5’-TCACCGGATCATGGCCAGCA-3’-3, which produced a 480-base pair band. β-globin was used as an internal positive control, which was amplified with the following primers: 5’-CAACTTCATCCACGTTCACC-3’ and 5’-GAAGAGCCAAGGACAGGTAC-3’ and produced a 268-base pair band. The primers were synthesized by Sangon and PCR amplifications were carried out in a Thermal Cycler (Perkin Elmer 4800). Main cycling parameters were 94 °C for 8 min, followed by 35 cycles of 94 °C for 30 s, 60 °C for 40 s and 72 °C for 1 min with a final extension at 72 °C for 10 min. PCR products were detected by electrophoresis in agarose gels (2 g·L-1 for GSTM1 and 12 g·L-1 for GSTT1).

Statistical analysis

The Chi-square method was used to test the frequencies of GSTM1 and GSTT1 genotypes. ORs and 95%CIs were calculated by logistic regression analysis controlling for possible confounding factors.


GSTM1 and GSTT1 null genotypes are indicated by the absence of a 157 bp band and 480 bp band, respectively. β-globin (268 bp) indicating the presence of DNA is co-amplified in all the samples (Figure 1, Figure 2).

Figure 1
Figure 1 Agarose gel electrophoresis of PCR products. 157 bp fragment: GSTM1; 268 bp fragment: β-globin. Lane M: marker; Lanes 4 and 5: GSTM1 null; Lanes 1, 2, 3, 6 and 7: GSTM1 non null.
Figure 2
Figure 2 Agarose gel electrophoresis of PCR products. 480 bp fragment: GSTT1; 268 bp fragment: β-globin. Lane M: marker; Lanes 1, 4, and 6: nun-null; Lanes 2, 3, 5 and 7: GSTT1 null.
Main characteristics of subjects

The main characteristics of cases and controls are presented in Table 1, the distribution of sex and age among cases and controls were not statistically significant (P > 0.05).

Table 1 Main characteristics of cases and controls.
Cases (n = 95)
Controls (n = 94)
Age groups/yr
< 5021(22.1)22(23.4)
≥ 7018(19.0)16(17.0)
Mean age59 ± 1158 ± 11
Age range32-7834-79
High school15(15.8)63(67.0)
Illiterate18(19.0)8( 8.5)
GSTM1 and GSTT1 genotype frequencies in cases and controls

The results showed that GSTM1 null genotype distributed unevenly between gastric cancer cases and controls. The frequency of GSTM1 null was significantly increased in gastric cancer cases compared with the general controls (χ2 = 5.75, P = 0.0165, Table 2).

Table 2 Association between GSTM1 and gastric cancer risk.
GSTM1 genotype
Crude OR (95%CI)2.03 (1.13-3.65)
Adjusted ORa (95%CI)2.03 (1.13-3.68)
Adjusted ORb (95%CI)2.47 (1.21-5.03)
Adjusted ORc (95%CI)2.63 (1.17-5.88)

Fifty percent (47/94) of individual in the controls exhibited the GSTT1 null genotype, and 43.2% (41/95) in gastric cancer cases. The frequencies of GSTT1 genotypes in cases and population controls were not significantly different (OR = 0.76, 95%CI 0.1-1.4). The odds ratio of gastric cancer associated with the combined genotypes of the polymorphisms of GSTM1 and GSTT1 are shown in Table 3. Persons who carried the GSTM1 null genotype and GSTT1 non-null had a higher risk of gastric cancer. The odds ratio was 2.77.

Table 3 Association between gastric cancer and combinations of GSTM1 and GSTT1 genotypes.
OR (95%CI)
Non-nullNull1414.72122.30.95 (0.36-2.50)
NullNull2728.42627.71.48 (0.64-3.47)
NullNon-null3334.71718.12.77 (1.15-6.77)
GSTM1 null genotype and smoking

Because GSTM1 may play an important role in the metabolism of tobacco smoke-derived carcinogens, the risk of gastric cancer associated with the polymophisms of metabolic enzymes may depend on the individuals’ smoking status. We compared smokers with and without gastric cancer and found that the increased susceptibility to gastric cancer in smokers with GSTM1 null phenotype. The subjects which have been exposed to cigarette smoking and GSTM1 null genotypes had 8.06 fold risk to develop gastric cancer (Table 4).

Table 4 Risk of gastric cancer in relation to GSTM1 genotypes by e smoking.
OR (95%CI)
NullNo3234.02223.21.60 (0.62-4.19)
NonnullYes2324.52324.22.33 (0.88-6.28)
NullYes1111.73840.08.06 (2.83-23.9)

Changle County is a hyperendemic area of gastric cancer. Familial aggregation of gastric cancer in this area has been reported in previous studies[15,16]. This familial tendency toward gastric cancer may result from a common environment shared by familial members of inherited genetic susceptibility[17]. Gastric cancer is a multistage process[18]. each caused by numbers of factors[19-31]. Environmental and host factors may all contribute to the etiology of gastric cancer[32]. The relationship between polymorphisms of genes involved in carcinogen metabolism and individual susceptibility to the mutagenic and carcinogenic actions of specific chemical exposure is a new field of research[33-35].

Recent studies reported genes that on code enzymes involved in the metabolism of carcioogens or environmental toxins may be related to an increased risk of cancer in some individuals[36,37]. GSTs are multifunctional proteins that catalyze many reactions between glutathione (GSH) and lipophilic compounds with electrophilic centers, including cytotoxic and genotoxic reactions[38]. Polycyclic aromatic hydrocarbons, N-nitrosomines, found in cigarette smoke and food, are potential human carcinogens[39,40]. Deficiency of detoxifying enzymes may affect the metabolic fates of these chemicals and raise cancer risks in exposed individuals[41]. The GSTM1 enzyme is involved in detoxifying a number of carcinogenic electrophiles, such as the epoxides of polycyclic aromatic hydrocarbons. Individuals with the homozygous GSTM1 null genotypes express no protein and are expected to have reduced abilities of detoxification of hazardous compounds, particularly epoxides.

In this study, GSTT1 gene deletion was not associated with gastric cancer. We observed evidence of a relationship between null genotype of GSTM1 and risk of gastric cancer. The GSTM1 genotype exhibited a higher frequency of gene deletions in cases than in controls. The finding suggests that GSTM1 may play a role in gastric cancer susceptibility. Gastric cancer, which is associated with exposure to smoking, may be more striking in individuals who carrying the null genotype GSTM1. This result suggests that intervention against smoking may be important for the prevention of gastric cancer in high incidence area because the GSTM1 is present in a majority of persons and the potential population impact may be important. However, these results should be considered preliminary. Larger studies will be needed to confirm potential gene-environment interactions.


Edited by Lu HM

1.  Zhang H, Ahmadi A, Arbman G, Zdolsek J, Carstensen J, Nordenskjöld B, Söderkvist P, Sun XF. Glutathione S-transferase T1 and M1 genotypes in normal mucosa, transitional mucosa and colorectal adenocarcinoma. Int J Cancer. 1999;84:135-138.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
2.  Setiawan VW, Zhang ZF, Yu GP, Li YL, Lu ML, Tsai CJ, Cordova D, Wang MR, Guo CH, Yu SZ. GSTT1 and GSTM1 null genotypes and the risk of gastric cancer: a case-control study in a Chinese population. Cancer Epidemiol Biomarkers Prev. 2000;9:73-80.  [PubMed]  [DOI]  [Cited in This Article: ]
3.  Dong CH, Yu SZ, Chen GC, Zhao DM, Hu Y. Association of polymorphisms of glutathione S-transferase M1 and T1 geno-types with elevated aflatoxin and increased risk of primary liver cancer. Huaren Xiaohua Zazhi. 1998;6:463-466.  [PubMed]  [DOI]  [Cited in This Article: ]
4.  Deng D, Chang Y, Li J. [Comparison of total N-nitrosamides in fasting gastric juice from subjects in high and low risk areas for gastric cancer]. Zhonghua Zhongliu Zazhi. 1997;19:96-99.  [PubMed]  [DOI]  [Cited in This Article: ]
5.  Harry XH. Association between Helicobacter pylori and gastric cancer: current knowledge and future research. World J Gastroenterol. 1998;4:93-96.  [PubMed]  [DOI]  [Cited in This Article: ]
6.  Wang SJ, Wen DG, Zhang J, Man X, Liu H. Intensify standardized therapy for esophageal and stomach cancer in tumor hospitals. World J Gastroenterol. 2001;7:80-82.  [PubMed]  [DOI]  [Cited in This Article: ]
7.  Wang Q, Jin PH, Lin GW, Xu SR. Cost-effectiveness of popula-tion-based Helicobacter pylori screening to prevent gastric cancer. Shijie Huaren Xiaohua Zazhi. 2000;8:262-265.  [PubMed]  [DOI]  [Cited in This Article: ]
8.  Niu WX, Qin XY, Liu H, Wang CP. Clinicopathological analysis of patients with gastric cancer in 1200 cases. World J Gastroenterol. 2001;7:281-284.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 28]  [Cited by in F6Publishing: 23]  [Article Influence: 1.0]  [Reference Citation Analysis (0)]
9.  Lu HD, Wang ZQ, Pan YR, Zhou TS, Xu XZ, Ke TW. Comparison of serum Zn, Cu and Se contents between healthy people and patients in high,middle and low incidence areas of gastric cancer of Fujian Province. World J Gastroenterol. 1999;5:84-86.  [PubMed]  [DOI]  [Cited in This Article: ]
10.  Chen Z, Zheng T, Chen J. [Evaluation of ten-year results of cancer prevention and treatment in Changle City with high incidence of gastric cancer]. Zhonghua Zhongliu Zazhi. 2000;22:311-313.  [PubMed]  [DOI]  [Cited in This Article: ]
11.  Cao GH, Yan SM, Yuan ZK, Wu L, Liu YF. A study of the relationship between trace element Mo and gastric cancer. World J Gastroenterol. 1998;4:55-56.  [PubMed]  [DOI]  [Cited in This Article: ]
12.  Cai L, Yu SZ, Ye WM, Yi YN. Fish sauce and gastric cancer: an ecological study in Fujian Province,China. World J Gastroenterol. 2000;6:671-675.  [PubMed]  [DOI]  [Cited in This Article: ]
13.  Cai L, Yu SZ, Zhang ZF. Helicobacter pylori infection and risk of gastric cancer in Changle County,Fujian Province,China. World J Gastroenterol. 2000;6:374-376.  [PubMed]  [DOI]  [Cited in This Article: ]
14.  Cai L, Yu SZ. A molecular epidemiologic study on gastric cancer in Changle, Fujian Province. Shijie Huaren Xiaohua Zazhi. 1999;7:652-655.  [PubMed]  [DOI]  [Cited in This Article: ]
15.  Ye WM, Yi YN, Luo RX, Zhou TS, Lin RT, Chen GD. Diet and gastric cancer: a casecontrol study in Fujian Province, China. World J Gastroenterol. 1998;4:516-518.  [PubMed]  [DOI]  [Cited in This Article: ]
16.  Wang ZQ, He J, Chen W, Chen Y, Zhou TS, Lin YC. Relationship between different sources of drinking water, water quality improvement and gastric cancer mortality in Changle County-A retrospective-cohort study in high incidence area. World J Gastroenterol. 1998;4:45-47.  [PubMed]  [DOI]  [Cited in This Article: ]
17.  Ottini L, Palli D, Falchetti M, D'Amico C, Amorosi A, Saieva C, Calzolari A, Cimoli F, Tatarelli C, De Marchis L. Microsatellite instability in gastric cancer is associated with tumor location and family history in a high-risk population from Tuscany. Cancer Res. 1997;57:4523-4529.  [PubMed]  [DOI]  [Cited in This Article: ]
18.  Wang GT. Progress in studies of mechanism of gastric precancerous lesions, carcinogenesis and their reversion. Shijie Huaren Xiaohua Zazhi. 2000;8:1-4.  [PubMed]  [DOI]  [Cited in This Article: ]
19.  Harrison LE, Zhang ZF, Karpeh MS, Sun M, Kurtz RC. The role of dietary factors in the intestinal and diffuse histologic subtypes of gastric adenocarcinoma: a case-control study in the U.S. Cancer. 1997;80:1021-1028.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 3]  [Reference Citation Analysis (0)]
20.  La Vecchia C, Muñoz SE, Braga C, Fernandez E, Decarli A. Diet diversity and gastric cancer. Int J Cancer. 1997;72:255-257.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 3]  [Reference Citation Analysis (0)]
21.  Ward MH, López-Carrillo L. Dietary factors and the risk of gastric cancer in Mexico City. Am J Epidemiol. 1999;149:925-932.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 99]  [Cited by in F6Publishing: 90]  [Article Influence: 3.6]  [Reference Citation Analysis (0)]
22.  Ward MH, Sinha R, Heineman EF, Rothman N, Markin R, Weisenburger DD, Correa P, Zahm SH. Risk of adenocarcinoma of the stomach and esophagus with meat cooking method and doneness preference. Int J Cancer. 1997;71:14-19.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 3]  [Reference Citation Analysis (0)]
23.  Zhang ZF, Kurtz RC, Marshall JR. Cigarette smoking and esophageal and gastric cardia adenocarcinoma. J Natl Cancer Inst. 1997;89:1247-1249.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 16]  [Cited by in F6Publishing: 16]  [Article Influence: 0.6]  [Reference Citation Analysis (0)]
24.  Ji BT, Chow WH, Yang G, McLaughlin JK, Zheng W, Shu XO, Jin F, Gao RN, Gao YT, Fraumeni JF. Dietary habits and stomach cancer in Shanghai, China. Int J Cancer. 1998;76:659-664.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 6]  [Reference Citation Analysis (0)]
25.  Hill MJ. Nutritional and metabolic aspects of gastrointestinal cancer. Curr Opin Clin Nutr Metab Care. 1998;1:405-407.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 10]  [Cited by in F6Publishing: 9]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
26.  Zhang ZF, Kurtz RC, Yu GP, Sun M, Gargon N, Karpeh M, Fein JS, Harlap S. Adenocarcinomas of the esophagus and gastric cardia: the role of diet. Nutr Cancer. 1997;27:298-309.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 151]  [Cited by in F6Publishing: 142]  [Article Influence: 6.2]  [Reference Citation Analysis (0)]
27.  Zhang ZF, Kurtz RC, Sun M, Karpeh M, Yu GP, Gargon N, Fein JS, Georgopoulos SK, Harlap S. Adenocarcinomas of the esophagus and gastric cardia: medical conditions, tobacco, alcohol, and socioeconomic factors. Cancer Epidemiol Biomarkers Prev. 1996;5:761-768.  [PubMed]  [DOI]  [Cited in This Article: ]
28.  Morgner A, Miehlke S, Stolte M, Neubauer A, Alpen B, Thiede C, Klann H, Hierlmeier FX, Ell C, Ehninger G. Development of early gastric cancer 4 and 5 years after complete remission of Helicobacter pylori-associated gastric low-grade marginal zone B-cell lymphoma of MALT type. World J Gastroenterol. 2001;7:248-253.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 52]  [Cited by in F6Publishing: 39]  [Article Influence: 1.7]  [Reference Citation Analysis (0)]
29.  Zhang ZW, Farthing MJ. Molecular mechanisms of H. pylori associated gastric carcinogenesis. World J Gastroenterol. 1999;5:369-374.  [PubMed]  [DOI]  [Cited in This Article: ]
30.  Jun Y, Fei G, Ebert MP, Malfertheiner P. Expression of inducible nitric oxide synthase in human gastric cancer. World J Gastroenterol. 1999;5:430-431.  [PubMed]  [DOI]  [Cited in This Article: ]
31.  Miehlke S, Kirsch C, Dragosics B, Gschwantler M, Oberhuber G, Antos D, Dite P, L-uter J, Labenz J, Leodolter A. Helicobacter pylori and gastric cancer: current status of the Austrian-Czech-German gastric cancer prevention trial (PRISMA-Study). World J Gastroenterol. 2001;7:243-247.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 37]  [Cited by in F6Publishing: 40]  [Article Influence: 1.7]  [Reference Citation Analysis (0)]
32.  Bartsch H, Nair U, Risch A, Rojas M, Wikman H, Alexandrov K. Genetic polymorphism of CYP genes, alone or in combination, as a risk modifier of tobacco-related cancers. Cancer Epidemiol Biomarkers Prev. 2000;9:3-28.  [PubMed]  [DOI]  [Cited in This Article: ]
33.  Harrison DJ, Hubbard AL, MacMillan J, Wyllie AH, Smith CA. Microsomal epoxide hydrolase gene polymorphism and susceptibility to colon cancer. Br J Cancer. 1999;79:168-171.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 52]  [Cited by in F6Publishing: 57]  [Article Influence: 2.3]  [Reference Citation Analysis (0)]
34.  Stücker I, de Waziers I, Cenée S, Bignon J, Depierre A, Milleron B, Beaune P, Hémon D. GSTM1, smoking and lung cancer: a case-control study. Int J Epidemiol. 1999;28:829-835.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 32]  [Cited by in F6Publishing: 32]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
35.  Slattery ML, Edwards SL, Samowitz W, Potter J. Associations between family history of cancer and genes coding for metabo-lizing enzymes (United States). Cancer Causes Control. 2000;11:799-803.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 19]  [Cited by in F6Publishing: 19]  [Article Influence: 0.8]  [Reference Citation Analysis (0)]
36.  Slattery ML, Kampman E, Samowitz W, Caan BJ, Potter JD. Interplay between dietary inducers of GST and the GSTM-1 genotype in colon cancer. Int J Cancer. 2000;87:728-733.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 2]  [Reference Citation Analysis (0)]
37.  Omer RE, Verhoef L, Van't Veer P, Idris MO, Kadaru AM, Kampman E, Bunschoten A, Kok FJ. Peanut butter intake, GSTM1 genotype and hepatocellular carcinoma: a case-control study in Sudan. Cancer Causes Control. 2001;12:23-32.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 35]  [Cited by in F6Publishing: 37]  [Article Influence: 1.6]  [Reference Citation Analysis (0)]
38.  London SJ, Yuan JM, Chung FL, Gao YT, Coetzee GA, Ross RK, Yu MC. Isothiocyanates, glutathione S-transferase M1 and T1 polymorphisms, and lung-cancer risk: a prospective study of men in Shanghai, China. Lancet. 2000;356:724-729.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 321]  [Cited by in F6Publishing: 326]  [Article Influence: 13.6]  [Reference Citation Analysis (0)]
39.  Guo XK, Wang TJ, Gu JF. Effect of esophagus and stomach cancer-preventing vinegar on N-nitrosoproline formation in human body. China Natl J New Gastroenterol. 1997;3:269-270.  [PubMed]  [DOI]  [Cited in This Article: ]
40.  Deng DJ, E Z. Overview on recent studies of gastric carcinogenesis: human exposure of N-nitrosamides. Shijie Huaren Xiaohua Zazhi. 2000;8:250-252.  [PubMed]  [DOI]  [Cited in This Article: ]
41.  Jourenkova-Mironova N, Voho A, Bouchardy C, Wikman H, Dayer P, Benhamou S, Hirvonen A. Glutathione S-transferase GSTM1, GSTM3, GSTP1 and GSTT1 genotypes and the risk of smoking-related oral and pharyngeal cancers. Int J Cancer. 1999;81:44-48.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]