|
|
|||
|
| |||
|
| |||
|
| |||
|
|
|||
|
Jin-Mei Piao, Min-Ho Shin, Jin-Su Choi, Department of Preventive Medicine, Chonnam National University Medical School, Gwangju 501-746, South Korea Sun-Seog Kweon, Jeonnam Regional Cancer Center, Chonnam National University Hwasun Hospital, Hwasun, Jeollanam-do 519-809, South Korea Hee Nam Kim, Genome Research Center for Hematopoietic Diseases, Chonnam National University Hwasun Hospital, Hwasun, Jeollanam-do 519-809, South Korea Woo-Kyun Bae, Hyun-Jeong Shim, Department of Hematology-Oncology, Chonnam National University Hwasun Hospital, Hwasun, Jeollanam-do 519-809, South Korea Hyeong-Rok Kim, Young-Kyu Park, Department of Surgery, Chonnam National University Hwasun Hospital, Hwasun, Jeollanam-do 519-809, South Korea Yoo-Duk Choi, Department of Pathology, Chonnam National University Medical School, Gwangju 501-746, South Korea Soo-Hyun Kim, Department of Laboratory Medicine, Chonnam National University Medical School, Gwangju 501-746, South Korea Author contributions: Piao JM designed the study, performed the majority of experiments, data analysis and interpretation and wrote the manuscript; Kim HN provided vital reagents and analytical tools and was also involved in editing the manuscript; Choi JS, Kweon SS and Kim SH provided the collection of all the DNA material and control sample; Bae WK, Shim HJ, Kim HR and Park YK collected clinical data; Choi YD collected clinicopathological data, Shin MH interpreted study findings, supervised the study and approved the final version of the manuscript. Correspondence to: Dr. Min-Ho Shin, Department of Preventive Medicine, Chonnam National University Medical School, 5, Hak1dong, Donggu, Gwangju City, 501-746, South Korea. mhshinx@paran.com Telephone: +82-62-2204166 Fax: +82-62-2330305 Received: September 3, 2009 Revised: October 15, 2009 Accepted: October 22, 2009 Published online: December 7, 2009
Abstract AIM: To evaluate the association of glutathione S-transferase mu (GSTM1) and glutathione S-transferase theta (GSTT1) null genotypes with the risk of gastric cancer (GC) and colorectal cancer (CRC) in a South Korean population.
METHODS: We conducted a population-based, large-scale case-control study including 2213 GCs, 1829 CRCs, and 1699 controls. Null and non-null genotypes of GSTM1 and GSTT1 were determined using real-time PCR.
RESULTS: The null genotypes of GSTM1 and GSTT1 were not significantly associated with elevated risk of gastric (OR = 1.070, 95% CI = 0.935-1.224; OR = 1.101, 95% CI = 0.963-1.259, respectively) or colorectal cancer (OR = 1.065, 95% CI = 0.923-1.228; OR = 1.041, 95% CI = 0.903-1.200, respectively). The frequency of the combined null GST genotype was not different between the two cancer groups and controls. Moreover, smoking, drinking, and age did not modify the association between these genotypes and the risk of gastric or colorectal cancer.
CONCLUSION: GSTM1 and GSTT1 null genotypes were not associated with increased risk of GC or CRC in Koreans.
© 2009 The WJG Press and Baishideng. All rights reserved.
Key words: Glutathione S-transferase mu; Glutathione S-transferase theta; Gastric cancer; Colorectal cancer; South Korean population
Peer reviewer: Dr. Mark S Pearce, Paediatric and Lifecourse Epidemiology Research Group, School of Clinical Medical Sciences, University of Newcastle, Sir James Spence Institute, Royal Victoria Infirmary, Newcastle upon Tyne, NE1 4LP, United Kingdom
Piao JM, Shin MH, Kweon SS, Kim HN, Choi JS, Bae WK, Shim HJ, Kim HR, Park YK, Choi YD, Kim SH. Glutathione-S-transferase (GSTM1, GSTT1) and the risk of gastrointestinal cancer in a Korean population. World J Gastroenterol 2009; 15(45): 5716-5721 Available from: URL: http://www.wjgnet.com/1007-9327/15/5716.asp DOI: http://dx.doi.org/10.3748/wjg.15.5716
INTRODUCTION Gastric cancer (GC) and colorectal cancer (CRC) are the most common malignancies in Korea. Environmental factors, such as diet, infection, and smoking, and genetic factors have been shown to play a role in the development of these malignancies[1-4]. Theglutathione S-transferase (GST) enzymes are involved in detoxification of many potentially carcinogenic compounds. The enzymes are encoded by at least five distantly related gene families (the alpha, mu, pi, sigma, and theta GSTs). In humans, marked interindividual differences exist in the expression of mu (GSTM1), and theta (GSTT1) GSTs[5]. The GSTM1 and GSTT1 null genotypes have been linked to increased risk of developing lung, bladder, colon, and skin cancers[5-7], and several studies have shown that GSTM1 and GSTT1 null genotypes were associated with increased risk of GC[8,9] and CRC[10]. However, some data have suggested that no relationship exists between the GSTM1 or GSTT1 null genotype and the risk of GC[11,12] or CRC[13,14]. The contradictory results regarding the association between GSTM1 and GSTT1 null genotypes and the risk of GC or CRC may be due to limited sample sizes or differences in the ethnicities or differences in the genetic subtypes studied, or they may also be attributable to differences in exposure to environmental factors. However, the majority of the reports involved small sample sizes, so the association of the GSTM1/GSTT1 null genotype and the risk of GC and CRC need to be confirmed in studies with larger numbers of samples. The present study aimed to evaluate the association of the GSTM1 and GSTT1 null genotypes with the risk of GC and CRC, and to determine whether smoking, alcohol consumption, and age modify the association between these polymorphisms and GC or CRC risk.
MATERIALS AND METHODS Ethics This study was approved by the Institutional Review Board of the Chonnam National University Hwasun Hospital in Hwasun, Korea, and all patients provided informed written consent.
Subjects Thestudy included 4042 newly diagnosed cancer cases (2213 GC and 1829 CRC) and 1699 controls. The cases were histologically confirmed at the Chonnam National University Hwasun Hospital (Jeollanam-do, Korea), between April 2004 and June 2008. Cases with secondary or recurrent tumors were excluded. The tumor stages were classified according to the TNM classification, including clinical or pathological TNM stages. GC was classified by anatomical site as cardia (C16.0) or non-cardia (C16.1-16.8) and by histological type as intestinal, diffuse, or mixed type. The control group (n = 1699) consisted of participants in the Thyroid Disease Prevalence Study conducted from July 2004 to January 2006 in Yeonggwang and Muan Counties of Jeollanam-do Province and in Namwon City of Jeollabuk-do, Korea[15]. At the time of peripheral blood collection, all case and control subjects provided their informed consent to participate in this study.
Blood samples and DNA isolation Blood samples were collected inEDTA-containing tubes, and DNA was extracted from the buffy coat for genotyping. Genomic DNA was extracted using a QIAamp DNA Blood Mini Kit (Qiagen, Valencia, CA) according to the manufacturer’s protocol.
Genotyping GSTM1 and GSTT1 genotyping was performed using a TaqMan allelic discrimination assay with previously described primers and modified probes[16]. Real-time PCR was performed using a Rotor-Gene 3000 multiplex system (Corbett Research, Sydney, Australia) in a 10-mL reaction volume containing 200 nmol/L PCR primer, 10 nmol/L CY5-labeled probe for GSTT1, 100 nmol/L FAM-labeled probe for GSTM1, 0.5 U of f-Taq polymerase (Solgent, Daejeon, Korea), and 40 ng of genomic DNA. The primer and probe are as follows: GSTM1, Forward, 5'-GGAGACAGAAGAGGAGAAGATTC-3', Reverse, 5'-GCCCAGCTGCATATGGTTGT-3', Probe, FAM-CCATGGTCTGGTTCTCCAAAATGTCCA-BHQ1; GSTT1, Forward, 5'-CTTCCAGGAGGCCCATGAG-3' Reverse, 5'-CAGGGCATCAGCTTCTGCTT-3', Probe, CY5-AAGGACTTCCCACCTGCAGACCCC-BHQ3.
Statistical analysis Statistical analysiswas performed using SPSS for Windows version 17.0. The descriptive data for the major characteristics of study groups are expressed as mean (range) and percent. We used t-tests to determine statistical differences in the continuous variables and c2 tests for the categorical variables. Adjusted odds ratios (OR) and their 95% confidence intervals (95% CI) were calculated using logistic regression models with adjustments for age and sex to estimate the association between genotype and GC or CRC. Interactions of genotype with smoking, alcohol consumption, and age were estimated using the logistic regression model, which included an interaction term as well as variables for exposure (smoking and alcohol drinking), genotypes, and potential confounders (sex and age). Subjects with wild-type genotypes were considered to have baseline risk. The subjects for which there was missing data for smoking, drinking, anatomical site, and histological type TNM staging were excluded in interaction analysis related with these variables. All tests were conducted at the P = 0.05 level of significance.
RESULTS We included 2213 cases of GC, 1829 cases of CRC, and 1699 cancer-free controls in the present study. The demographic characteristics of subjects are shown in Table 1. The proportion of men in the cancer cases was higher than that in the controls, and cases in both cancer groups tended to be older than controls. The proportion of smoking in GC cases was higher than that in the controls, but in CRC cases was lower than that in the controls. The proportion of drinking in both cancer groups was lower than that in the controls. The frequency distributions of the GSTM1 null genotype in the control, GC, and CRC groups were 54.3%, 55.4%, and 54.9%, respectively. The frequency distributions of the GSTT1 null genotype in the control, GC, and CRC groups were 50.5%, 53.0%, and 51.9%, respectively. No significant differences were observed in the frequencies of the GSTT1 and GSTM1 genotypes between cancer patients and controls (Table 1). The GSTM1 and GSTT1 null genotypes were not significantly associated with risk of GC (OR = 1.070, 95% CI = 0.935-1.224; OR = 1.101, 95% CI = 0.963-1.259, respectively) or CRC (OR = 1.065, 95% CI = 0.923-1.228; OR = 1.041, 95% CI = 0.903-1.200, respectively). The GSTM1 and GSTT1 null genotypes were not significantly associated with the risk of GC or CRC, classified according to TNM stage, tumor site or histology type (GC) (Tables 2 and 3). Smoking, alcohol consumption and age did not modify the association between the GSTM1 and GSTT1 null genotypes and the risk of GC or CRC (Tables 2 and 3). No difference in the frequency of the combined GSTM1 and GSTT1 null genotype was observed between the two cancer groups and controls (Table 4).
DISCUSSION The present large-scale study investigated the association between GSTM1 and GSTT1 null genotypes and susceptibility to GC and CRC in a South Korean population. In this study, we observed no significant association between either type of cancer and the GSTM1 and GSTT1 null genotypes. Additionally, no difference was observed in the frequency of the combined GST (M1 and T1) null genotype between the two cancer groups and controls. Moreover, smoking did not modify the association between these polymorphisms and risk of GC or CRC. The reports examining the GSTM1 and GSTT1 null genotypes and their association with gastric cancer are quite inconsistent. Two reports suggested that the GSTM1 null genotype increased GC risk[8,10], and three reported that the GSTT1 null genotype increased GC risk[9,17,18]. However, our results suggest that no associations exist which is in line with the majority of reports[11,12,19-21]. In studies of Korean populations, no significant associations were detected between the GSTM1 and GSTT1 null genotypes and GC risk. One study conducted in Iksan, Korea, reported that the GSTM1 and GSTT1 null genotypes had no association with the risk of GC (for GSTM1 null, OR = 0.86 and 95% CI = 0.49-1.51; for GSTT1 null, OR = 0.97 and 95% CI = 0.55-1.71)[12]. Hong et al[20] reported similar results. Another study suggested that the GSTM1 and GSTT1 null genotypes were not associated with the risk of GC overall, but that in individuals who consumed kimchi, a spicy Korean food made with fermented cabbage, the GSTM1 and GSTT1 non-null genotype increased the risk of GC[19]. Two meta-analyses, by La Torre et al[22] and Boccia et al[23] suggested that the GSTM1 and GSTT1 null genotypes have no effect on the risk of GC per se, but may modulate tobacco-related carcinogenesis of gastric cancer. Two studies reported that the GSTT1 null genotype increased the risk of CRC[10,24], and three studies reported decreased CRC risk, one for the GSTM1 null[25] and two for the GSTT1 null genotype[26,27]. However, five studies suggested that the GSTM1 and GSTT1 null genotype are not related to CRC risk[4,8,13,14,28]. One Korean study suggested that the genotypes of GSTM1 are associated with cancer occurrence in individuals carrying the hMLH1/hMSH2 mutation who were family members of patients with hereditary nonpolyposis colorectal cancer[29]. The conflicting results regarding the associations between GSTM1 and GSTT1 null genotypes and risks for GC and CRC may be due to limited sample size or differences in the ethnicities or genetic subtypes studied, and they may also be attributable to differences in exposure to environmental factors. Polycyclic aromatic hydrocarbons (PAHs) are the main carcinogens in tobacco smoke. The ultimate carcinogen (PAH-DE) can be detoxified through conjugation with glutathione by GSTs, which are phase Ⅱ enzymes[30]. Individuals with the null genotype of GSTM1 or GSTT1 would have less capacity for detoxification of PAHs, which would potentially increase their risk of chemical carcinogenesis. However, our data suggested that smoking did not modify the association between the GSTM1 and GSTT1 null genotypes and the risk of GC or CRC. Four studies examined the interaction between smoking, GSTM1 or GSTT1 polymorphisms, and the risk of GC[10,11,18,21]. One study suggested that smoking modifies the association between the GSTM1 null genotype and the risk of GC[21]. In contrast, three studies reported that smoking did not modify the association between the GSTM1 and/or GSTT1 null genotype and GC risk[10,11,18], in line with our results. Additionally, six studies evaluated the interaction between smoking, the GSTM1 or GSTT1 null genotype, and the risk of CRC[13,25,31-34]. Two studies reported that smoking modifies the association between the GSTM1 and/or GSTT1 null genotype and CRC risk[13,31]. However, four studies reported no interaction between the GSTM1 and/or GSTT1 null genotype and smoking in CRC risk[25,32-34], in agreement with our results. Our study suggests that alcohol consumption did not modify the association of GSTM1 and GSTT1 null genotypes with the risk of GC or CRC, which is consistent with previous studies regarding GC[9,11,18]. However, no studies have been reported examining whether alcohol consumption modifies the association of the GSTM1 or GSTT1 null genotype with the risk of CRC. The detoxification potential of the GSTs was observed to decrease with age[35]. Yeh et al[24] reported that men aged ≤ 60 years with the GSTT1 null genotype were at significantly increased risk of rectal cancer, and one study reported the GSTT1 null genotype was not associated with the risk of GC, classified according to age less than or greater than 60 years[17]. However, the present study suggested that age does not modify the association between GSTM1 and GSTT1 null genotypes and the risk of GC or CRC. In our data, the GSTM1 and GSTT1 null genotypes were not significantly associated with the risk of GC or CRC, classified according to TNM stage, tumor site, and histology type (GC). To the best of our knowledge, no reports have been published regarding the GSTM1 and GSTT1 null genotypes and GC or CRC risk classified according to TNM stage. Two studies investigated the association between the GSTM1 and GSTT1 null genotypes and the risk of cardia or non-cardia GC, and both studies suggested that no significant association exists[3,36], in line with our result. Seow et al[37] reported that the GSTM1 and GSTT1 null genotypes were not associated with the risk of CRC, classified according to location of the tumor in the colon or the rectum. Suzuki et al[38] reported finding no association between the GSTM1 null genotype and the risk of intestinal type or diffuse type GC, and Agudo et al[3] reported finding no association between the GSTT1 null genotype and the risk of intestinal type or diffuse type GC, consistent with our results. In our data, smoking was associated with increased risk of GC, but with decreased risk of CRC. Previous studies reported that smoking increased the risk of GC[39], in line with our results. The association between smoking and CRC has been inconsistent among studies. A recent meta-analysis suggested that smoking is significantly associated with CRC incidence[40]. In our data, drinking was associated with decreased risk of both cancer groups. Drinking probably does not affect overall risk of stomach cancer, but there is some evidence that drinking may increase the risk of GC[41]. The relationship between drinking and CRC risk has been controversial, but a meta-analysis found that high consumers of alcohol had an elevated CRC risk[42]. We could not rule out the possibility that differential misclassification bias may have occurred in our study, because we retrospectively gathered information about smoking and drinking from electronic medical records in both case groups, while cross-sectional surveys were used to gather information about smoking and alcohol in controls. The major strength of our study was its large sample size. Ours was the first investigation of the risk of GC and CRC according to the GSTM1 and GSTT1 null genotypes in a large Korean population. The limitations of our study must also be acknowledged. First, the study did not consider genetic polymorphisms of other cancer related genes. Second, the study considered a limited number of environmental factors (smoking and alcohol consumption), and other environmental factors such as dietary intake were not considered. In conclusion, the results of the present population-based, large-scale case-control study suggest that in a Korean population, the GSTM1/GSTT1 null genotype does not modulate an individual’s susceptibility to GC or CRC, and that smoking, alcohol consumption, and age do not modify the association between these genotypes and the risk of GC or CRC.
COMMENTS Background Gastric cancer (GC) and colorectal cancer (CRC) are the most common malignancies in Korea. Environmental factors and genetic factors have been shown to play a role in the development of these malignancies. Research frontiers The glutathione S-transferase enzymes are involved in detoxification of many potentially carcinogenic compounds. Several studies have shown that glutathione S-transferase mu (GSTM1) and glutathione S-transferase theta (GSTT1) null genotypes were associated with increased risks for GC and CRC. But some data suggested no relationship between GSTM1/GSTT1 null genotype and the risk of GC and CRC. Innovations and breakthroughs This is the first investigation of the risk of GC and CRC according to the GSTM1 and GSTT1 null genotypes in a large Korean population. It also aimed to determine whether smoking, alcohol consumption, and age modify the association between these polymorphisms and GC or CRC risk. Applications This study suggested that GSTM1 and GSTT1 null genotypes were not associated with increased risk of GC or CRC in Koreans. Smoking, drinking, and age did not modify the association between these genotypes and the risk of gastric or colorectal cancer. Future research should focus on other parts of the GST genotype to understand its role and risk of gastric and colorectal cancer in Korean population. Terminology GST: Glutathione-S-transferase is a Phase Ⅱ detoxification enzyme. The enzymes are encoded by at least five distantly related gene families (the alpha, mu, pi, sigma, and theta GSTs). In humans, marked interindividual differences exist in the expression of mu (GSTM1), and theta (GSTT1) GSTs. Peer review This is the first investigation of the risk of GC and CRC according to the GSTM1 and GSTT1 null genotypes in a large Korean population. It also determined whether smoking, alcohol consumption, and age modify the association between these polymorphisms and GC or CRC risk. Although results of this study show no association between the null genotypes of GSTM1 and GSTT1 and risk of gastric and colorectal cancer, and no-association results are not as attractive as positive associations, I feel they should be presented to the scientific audience in order not to create a literature bias towards publishing only studies with positive associations.
REFERENCES 1 Correa P. Human gastric carcinogenesis: a multistep and multifactorial process--First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992; 52: 6735-6740 PubMed 2 Gonzalez CA, Sala N, Capella G. Genetic susceptibility and gastric cancer risk. Int J Cancer 2002; 100: 249-260 PubMed DOI 3 Agudo A, Sala N, Pera G, Capella G, Berenguer A, Garcia N, Palli D, Boeing H, Del Giudice G, Saieva C, Carneiro F, Berrino F, Sacerdote C, Tumino R, Panico S, Berglund G, Siman H, Stenling R, Hallmans G, Martinez C, Bilbao R, Barricarte A, Navarro C, Quiros JR, Allen N, Key T, Bingham S, Khaw KT, Linseisen J, Nagel G, Overvad K, Tjonneland A, Olsen A, Bueno-de-Mesquita HB, Boshuizen HC, Peeters PH, Numans ME, Clavel-Chapelon F, Boutron-Ruault MC, Trichopoulou A, Lund E, Offerhaus J, Jenab M, Ferrari P, Norat T, Riboli E, Gonzalez CA. Polymorphisms in metabolic genes related to tobacco smoke and the risk of gastric cancer in the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomarkers Prev 2006; 15: 2427-2434 PubMed DOI 4 Little J, Sharp L, Masson LF, Brockton NT, Cotton SC, Haites NE, Cassidy J. Colorectal cancer and genetic polymorphisms of CYP1A1, GSTM1 and GSTT1: a case-control study in the Grampian region of Scotland. Int J Cancer 2006; 119: 2155-2164 PubMed DOI 5 Hayes JD, Pulford DJ. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol 1995; 30: 445-600 PubMed DOI 6 Nakajima T, Elovaara E, Anttila S, Hirvonen A, Camus AM, Hayes JD, Ketterer B, Vainio H. Expression and polymorphism of glutathione S-transferase in human lungs: risk factors in smoking-related lung cancer. Carcinogenesis 1995; 16: 707-711 PubMed DOI 7 Bell DA, Taylor JA, Paulson DF, Robertson CN, Mohler JL, Lucier GW. Genetic risk and carcinogen exposure: a common inherited defect of the carcinogen-metabolism gene glutathione S-transferase M1 (GSTM1) that increases susceptibility to bladder cancer. J Natl Cancer Inst 1993; 85: 1159-1164 PubMed DOI 8 Saadat I, Saadat M. Glutathione S-transferase M1 and T1 null genotypes and the risk of gastric and colorectal cancers. Cancer Lett 2001; 169: 21-26 PubMed DOI 9 Setiawan VW, Zhang ZF, Yu GP, Li YL, Lu ML, Tsai CJ, Cordova D, Wang MR, Guo CH, Yu SZ, Kurtz RC. 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 10 Katoh T, Nagata N, Kuroda Y, Itoh H, Kawahara A, Kuroki N, Ookuma R, Bell DA. Glutathione S-transferase M1 (GSTM1) and T1 (GSTT1) genetic polymorphism and susceptibility to gastric and colorectal adenocarcinoma. Carcinogenesis 1996; 17: 1855-1859 PubMed DOI 11 Gao CM, Takezaki T, Wu JZ, Li ZY, Liu YT, Li SP, Ding JH, Su P, Hu X, Xu TL, Sugimura H, Tajima K. Glutathione-S-transferases M1 (GSTM1) and GSTT1 genotype, smoking, consumption of alcohol and tea and risk of esophageal and stomach cancers: a case-control study of a high-incidence area in Jiangsu Province, China. Cancer Lett 2002; 188: 95-102 PubMed DOI 12 Choi SC, Yun KJ, Kim TH, Kim HJ, Park SG, Oh GJ, Chae SC, Oh GJ, Nah YH, Kim JJ, Chung HT. Prognostic potential of glutathione S-transferase M1 and T1 null genotypes for gastric cancer progression. Cancer Lett 2003; 195: 169-175 PubMed 13 Epplein M, Wilkens LR, Tiirikainen M, Dyba M, Chung FL, Goodman MT, Murphy SP, Henderson BE, Kolonel LN, Le Marchand L. Urinary isothiocyanates; glutathione S-transferase M1, T1, and P1 polymorphisms; and risk of colorectal cancer: the Multiethnic Cohort Study. Cancer Epidemiol Biomarkers Prev 2009; 18: 314-320 PubMed DOI 14 Inoue H, Kiyohara C, Shinomiya S, Marugame T, Tsuji E, Handa K, Hayabuchi H, Eguchi H, Fukushima Y, Kono S. Glutathione S-transferase polymorphisms and risk of colorectal adenomas. Cancer Lett 2001; 163: 201-206 PubMed DOI 15 Kim HN, Lee IK, Kim YK, Tran HT, Yang DH, Lee JJ, Shin MH, Park KS, Shin MG, Choi JS, Kim HJ. Association between folate-metabolizing pathway polymorphism and non-Hodgkin lymphoma. Br J Haematol 2008; 140: 287-294 PubMed DOI 16 Ashton LJ, Murray JE, Haber M, Marshall GM, Ashley DM, Norris MD. Polymorphisms in genes encoding drug metabolizing enzymes and their influence on the outcome of children with neuroblastoma. Pharmacogenet Genomics 2007; 17: 709-717 PubMed DOI 17 Palli D, Saieva C, Gemma S, Masala G, Gomez-Miguel MJ, Luzzi I, D'Errico M, Matullo G, Ozzola G, Manetti R, Nesi G, Sera F, Zanna I, Dogliotti E, Testai E. GSTT1 and GSTM1 gene polymorphisms and gastric cancer in a high-risk italian population. Int J Cancer 2005; 115: 284-289 PubMed DOI 18 Boccia S, Sayed-Tabatabaei FA, Persiani R, Gianfagna F, Rausei S, Arzani D, La Greca A, D'Ugo D, La Torre G, van Duijn CM, Ricciardi G. Polymorphisms in metabolic genes, their combination and interaction with tobacco smoke and alcohol consumption and risk of gastric cancer: a case-control study in an Italian population. BMC Cancer 2007; 7: 206 PubMed DOI 19 Nan HM, Park JW, Song YJ, Yun HY, Park JS, Hyun T, Youn SJ, Kim YD, Kang JW, Kim H. Kimchi and soybean pastes are risk factors of gastric cancer. World J Gastroenterol 2005; 11: 3175-3181 PubMed 20 Hong SH, Kim JW, Kim HG, Park IK, Ryoo JW, Lee CH, Sohn YK, Lee JY. [Glutathione S-transferases (GSTM1, GSTT1 and GSTP1) and N-acetyltransferase 2 polymorphisms and the risk of gastric cancer] J Prev Med Public Health 2006; 39: 135-140 PubMed 21 Li H, Chen XL, Li HQ. Polymorphism of CYPIA1 and GSTM1 genes associated with susceptibility of gastric cancer in Shandong Province of China. World J Gastroenterol 2005; 11: 5757-5762 PubMed 22 La Torre G, Boccia S, Ricciardi G. Glutathione S-transferase M1 status and gastric cancer risk: a meta-analysis. Cancer Lett 2005; 217: 53-60 PubMed DOI 23 Boccia S, La Torre G, Gianfagna F, Mannocci A, Ricciardi G. Glutathione S-transferase T1 status and gastric cancer risk: a meta-analysis of the literature. Mutagenesis 2006; 21: 115-123 PubMed DOI 24 Yeh CC, Hsieh LL, Tang R, Chang-Chieh CR, Sung FC. Vegetable/fruit, smoking, glutathione S-transferase polymorphisms and risk for colorectal cancer in Taiwan. World J Gastroenterol 2005; 11: 1473-1480 PubMed 25 Moore LE, Huang WY, Chatterjee N, Gunter M, Chanock S, Yeager M, Welch B, Pinsky P, Weissfeld J, Hayes RB. GSTM1, GSTT1, and GSTP1 polymorphisms and risk of advanced colorectal adenoma. Cancer Epidemiol Biomarkers Prev 2005; 14: 1823-1827 PubMed DOI 26 Huang K, Sandler RS, Millikan RC, Schroeder JC, North KE, Hu J. GSTM1 and GSTT1 polymorphisms, cigarette smoking, and risk of colon cancer: a population-based case-control study in North Carolina (United States). Cancer Causes Control 2006; 17: 385-394 PubMed DOI 27 Probst-Hensch NM, Sun CL, Van Den Berg D, Ceschi M, Koh WP, Yu MC. The effect of the cyclin D1 (CCND1) A870G polymorphism on colorectal cancer risk is modified by glutathione-S-transferase polymorphisms and isothiocyanate intake in the Singapore Chinese Health Study. Carcinogenesis 2006; 27: 2475-2482 PubMed DOI 28 van der Logt EM, Bergevoet SM, Roelofs HM, van Hooijdonk Z, te Morsche RH, Wobbes T, de Kok JB, Nagengast FM, Peters WH. Genetic polymorphisms in UDP-glucuronosyltransferases and glutathione S-transferases and colorectal cancer risk. Carcinogenesis 2004; 25: 2407-2415 PubMed DOI 29 Shin JH, Ku JL, Shin KH, Shin YK, Kang SB, Park JG. Glutathione S-transferase M1 associated with cancer occurrence in Korean HNPCC families carrying the hMLH1/hMSH2 mutation. Oncol Rep 2003; 10: 483-486 PubMed 30 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 31 Gertig DM, Stampfer M, Haiman C, Hennekens CH, Kelsey K, Hunter DJ. Glutathione S-transferase GSTM1 and GSTT1 polymorphisms and colorectal cancer risk: a prospective study. Cancer Epidemiol Biomarkers Prev 1998; 7: 1001-1005 PubMed 32 Slattery ML, Curtin K, Ma K, Schaffer D, Potter J, Samowitz W. GSTM-1 and NAT2 and genetic alterations in colon tumors. Cancer Causes Control 2002; 13: 527-534 PubMed DOI 33 Luchtenborg M, Weijenberg MP, Kampman E, van Muijen GN, Roemen GM, Zeegers MP, Goldbohm RA, van 't Veer P, de Goeij AF, van den Brandt PA. Cigarette smoking and colorectal cancer: APC mutations, hMLH1 expression, and GSTM1 and GSTT1 polymorphisms. Am J Epidemiol 2005; 161: 806-815 PubMed DOI 34 Lin HJ, Probst-Hensch NM, Ingles SA, Han CY, Lin BK, Lee DB, Frankl HD, Lee ER, Longnecker MP, Haile RW. Glutathione transferase (GSTM1) null genotype, smoking, and prevalence of colorectal adenomas. Cancer Res 1995; 55: 1224-1226 PubMed 35 van Lieshout EM, Peters WH. Age and gender dependent levels of glutathione and glutathione S-transferases in human lymphocytes. Carcinogenesis 1998; 19: 1873-1875 PubMed DOI 36 Wideroff L, Vaughan TL, Farin FM, Gammon MD, Risch H, Stanford JL, Chow WH. GST, NAT1, CYP1A1 polymorphisms and risk of esophageal and gastric adenocarcinomas. Cancer Detect Prev 2007; 31: 233-236 PubMed DOI 37 Seow A, Yuan JM, Sun CL, Van Den Berg D, Lee HP, Yu MC. Dietary isothiocyanates, glutathione S-transferase polymorphisms and colorectal cancer risk in the Singapore Chinese Health Study. Carcinogenesis 2002; 23: 2055-2061 PubMed DOI 38 Suzuki S, Muroishi Y, Nakanishi I, Oda Y. Relationship between genetic polymorphisms of drug-metabolizing enzymes (CYP1A1, CYP2E1, GSTM1, and NAT2), drinking habits, histological subtypes, and p53 gene point mutations in Japanese patients with gastric cancer. J Gastroenterol 2004; 39: 220-230 PubMed DOI 39 Siman JH, Forsgren A, Berglund G, Floren CH. Tobacco smoking increases the risk for gastric adenocarcinoma among Helicobacter pylori-infected individuals. Scand J Gastroenterol 2001; 36: 208-213 PubMed DOI 40 Botteri E, Iodice S, Bagnardi V, Raimondi S, Lowenfels AB, Maisonneuve P. Smoking and colorectal cancer: a meta-analysis. JAMA 2008; 300: 2765-2778 PubMed 41 Terry MB, Gaudet MM, Gammon MD. The epidemiology of gastric cancer. Semin Radiat Oncol 2002; 12: 111-127 PubMed 42 Bagnardi V, Blangiardo M, La Vecchia C, Corrao G. Alcohol consumption and the risk of cancer: a meta-analysis. Alcohol Res Health 2001; 25: 263-270 PubMed
S- Editor Tian L L- Editor O'Neill M E- Editor Ma WH
| |||
| |||||||
|
|
