Molecular Biology Reports

, Volume 40, Issue 3, pp 2397–2403 | Cite as

Significant association of glutathione S-transferase T1 null genotype with esophageal cancer risk: a meta-analysis

Article

Abstract

Recent studies on the association between glutathione S-transferase T1 (GSTT1) polymorphism and risk of esophageal cancer showed inconclusive results. To clarify this possible association, we conducted a meta-analysis of published studies. Data were collected from the following electronic databases: Pubmed, Embase, and Chinese Biomedical Database (CBM). The odds ratio (OR) and its 95 % confidence interval (95 % CI) was used to assess the strength of this association. We summarized the data on the association between GSTT1 null genotype and risk of esophageal cancer in the overall population, and performed subgroup analyses by ethnicity. Finally, a total of 24 independent studies including a total of 7,801 subjects (2,965 cases and 4,836 controls) were eligible for meta-analysis. In the overall analysis, there was no significant association between GSTT1 null genotype and esophageal cancer risk (OR = 1.15, 95 % CI 0.99–1.33, P = 0.067). However, meta-analysis of adjusted ORs showed a significant association between GSTT1 null genotype and increased risk of esophageal cancer (OR = 1.30, 95 % CI 1.08–1.56, P = 0.005). Subgroup analyses by ethnicity showed there was an obvious association between GSTT1 null genotype and increased risk of esophageal cancer in East Asians (OR = 1.24, 95 % CI 1.10–1.39, P < 0.001), but not in Caucasians (OR = 0.89, 95 % CI 0.71–1.11, P = 0.300). There was no obvious risk of publication bias in this meta-analysis (Egger’s test, P = 0.784). This meta-analysis demonstrates that GSTT1 null genotype is independently associated with increased risk of esophageal cancer, and a race-specific effect may exist in this association.

Keywords

Esophageal cancer GSTT1 Meta-analysis Polymorphism 

Abbreviations

GSTs

Glutathione S-transferases

GSTT1

Glutathione S-transferase T1

95 % CI

95 % confidence interval

OR

Odds ratio

References

  1. 1.
    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69–90PubMedCrossRefGoogle Scholar
  2. 2.
    Enzinger PC, Mayer RJ (2003) Esophageal cancer. N Engl J Med 349:2241–2252PubMedCrossRefGoogle Scholar
  3. 3.
    Chen WQ (2009) Estimation of cancer incidence and mortality in China in 2004–2005. Chin J Oncol 31:664–668Google Scholar
  4. 4.
    Hvid-Jensen F, Pedersen L, Drewes AM, Sorensen HT, Funch-Jensen P (2011) Incidence of adenocarcinoma among patients with Barrett’s esophagus. N Engl J Med 365:1375–1383PubMedCrossRefGoogle Scholar
  5. 5.
    Hiyama T, Yoshihara M, Tanaka S, Chayama K (2007) Genetic polymorphisms and esophageal cancer risk. Int J Cancer 121:1643–1658PubMedCrossRefGoogle Scholar
  6. 6.
    Dong LM, Potter JD, White E, Ulrich CM, Cardon LR, Peters U (2008) Genetic susceptibility to cancer: the role of polymorphisms in candidate genes. JAMA 299:2423–2436PubMedCrossRefGoogle Scholar
  7. 7.
    Xiong G, Guo H, Wang K, Hu H, Wang D, Xu X, Guan X, Yang K, Bai Y (2010) Polymorphisms of decoy receptor 3 are associated with risk of esophageal squamous cell carcinoma in Chinese Han. Tumour Biol 31:443–449PubMedCrossRefGoogle Scholar
  8. 8.
    Liu J, Li Z, Cui J, Xu G, Cui G (2012) Cellular changes in the tumor microenvironment of human esophageal squamous cell carcinomas. Tumour Biol 33:495–505PubMedCrossRefGoogle Scholar
  9. 9.
    Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51–88PubMedCrossRefGoogle Scholar
  10. 10.
    Sharma R, Yang Y, Sharma A, Awasthi S, Awasthi YC (2004) Antioxidant role of glutathione S-transferases: protection against oxidant toxicity and regulation of stress-mediated apoptosis. Antioxid Redox Signal 6:289–300PubMedCrossRefGoogle Scholar
  11. 11.
    Strange RC, Spiteri MA, Ramachandran S, Fryer AA (2001) Glutathione-S-transferase family of enzymes. Mutat Res 482:21–26PubMedCrossRefGoogle Scholar
  12. 12.
    Hayes JD, Strange RC (2000) Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology 61:154–166PubMedCrossRefGoogle Scholar
  13. 13.
    Katoh T, Yamano Y, Tsuji M, Watanabe M (2008) Genetic polymorphisms of human cytosol glutathione S-transferases and prostate cancer. Pharmacogenomics 9:93–104PubMedCrossRefGoogle Scholar
  14. 14.
    Lin DX, Tang YM, Peng Q, Lu SX, Ambrosone CB, Kadlubar FF (1998) Susceptibility to esophageal cancer and genetic polymorphisms in glutathione S-transferases t1, p1, and m1 and cytochrome p450 2e1. Cancer Epidemiol Biomarkers Prev 7:1013–1018PubMedGoogle Scholar
  15. 15.
    van Lieshout EM, Roelofs HM, Dekker S, Mulder CJ, Wobbes T, Jansen JB, Peters WH (1999) Polymorphic expression of the glutathione S-transferase p1 gene and its susceptibility to Barrett’s esophagus and esophageal carcinoma. Cancer Res 59:586–589PubMedGoogle Scholar
  16. 16.
    Tan W, Song N, Wang GQ, Liu Q, Tang HJ, Kadlubar FF, Lin DX (2000) Impact of genetic polymorphisms in cytochrome p450 2e1 and glutathione S-transferases m1, t1, and p1 on susceptibility to esophageal cancer among high-risk individuals in China. Cancer Epidemiol Biomarkers Prev 9:551–556PubMedGoogle Scholar
  17. 17.
    Gao CM, Takezaki T, Wu JZ, Li ZY, Liu YT, Li SP, Ding JH, Su P, Hu X, Xu TL, Sugimura H, Tajima K (2002) 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 188:95–102PubMedCrossRefGoogle Scholar
  18. 18.
    Casson AG, Zheng Z, Chiasson D, MacDonald K, Riddell DC, Guernsey JR, Guernsey DL, McLaughlin J (2003) Associations between genetic polymorphisms of phase I and II metabolizing enzymes, p53 and susceptibility to esophageal adenocarcinoma. Cancer Detect Prev 27:139–146PubMedCrossRefGoogle Scholar
  19. 19.
    Roth MJ, Abnet CC, Johnson LL, Mark SD, Dong ZW, Taylor PR, Dawsey SM, Qiao YL (2004) Polymorphic variation of cyp1a1 is associated with the risk of gastric cardia cancer: a prospective case–cohort study of cytochrome p-450 1a1 and gst enzymes. Cancer Causes Control 15:1077–1083PubMedCrossRefGoogle Scholar
  20. 20.
    Casson AG, Zheng Z, Porter GA, Guernsey DL (2006) Genetic polymorphisms of microsomal epoxide hydroxylase and glutathione S-transferases m1, t1 and p1, interactions with smoking, and risk for esophageal (Barrett) adenocarcinoma. Cancer Detect Prev 30:423–431PubMedCrossRefGoogle Scholar
  21. 21.
    Jain M, Kumar S, Rastogi N, Lal P, Ghoshal UC, Tiwari A, Pant MC, Baiq MQ, Mittal B (2006) Gstt1, gstm1 and gstp1 genetic polymorphisms and interaction with tobacco, alcohol and occupational exposure in esophageal cancer patients from North India. Cancer Lett 242:60–67PubMedCrossRefGoogle Scholar
  22. 22.
    Wang Z, Tang L, Sun G, Tang Y, Xie Y, Wang S, Hu X, Gao W, Cox SB, Wang JS (2006) Etiological study of esophageal squamous cell carcinoma in an endemic region: a population-based case control study in Huaian, China. BMC Cancer 6:287PubMedCrossRefGoogle Scholar
  23. 23.
    Rossini A, Rapozo DC, Soares Lima SC, Guimaraes DP, Ferreira MA, Teixeira R, Kruel CD, Barros SG, Andreollo NA, Acatauassu R, Matos HJ, Albano RM, Pinto LF (2007) Polymorphisms of gstp1 and gstt1, but not of cyp2a6, cyp2e1 or gstm1, modify the risk for esophageal cancer in a western population. Carcinogenesis 28:2537–2542PubMedCrossRefGoogle Scholar
  24. 24.
    Matejcic M, Li D, Prescott NJ, Lewis CM, Mathew CG, Parker MI (2011) Association of a deletion of gstt2b with an altered risk of oesophageal squamous cell carcinoma in a South African population: a case–control study. PLoS ONE 6:e29366PubMedCrossRefGoogle Scholar
  25. 25.
    Mantel N, Haenszel W (1959) Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 22:719–748PubMedGoogle Scholar
  26. 26.
    DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188PubMedCrossRefGoogle Scholar
  27. 27.
    Cochran WG (1954) The combination of estimates from different experiments. Biometrics 10:101–129CrossRefGoogle Scholar
  28. 28.
    Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560PubMedCrossRefGoogle Scholar
  29. 29.
    Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634PubMedCrossRefGoogle Scholar
  30. 30.
    Li D, Dandara C, Parker MI (2010) The 341c/t polymorphism in the gstp1 gene is associated with increased risk of oesophageal cancer. BMC Genet 11:47PubMedCrossRefGoogle Scholar
  31. 31.
    Zendehdel K, Bahmanyar S, McCarthy S, Nyren O, Andersson B, Ye W (2009) Genetic polymorphisms of glutathione S-transferase genes gstp1, gstm1, and gstt1 and risk of esophageal and gastric cardia cancers. Cancer Causes Control 20:2031–2038PubMedCrossRefGoogle Scholar
  32. 32.
    Wideroff L, Vaughan TL, Farin FM, Gammon MD, Risch H, Stanford JL, Chow WH (2007) Gst, nat1, cyp1a1 polymorphisms and risk of esophageal and gastric adenocarcinomas. Cancer Detect Prev 31:233–236PubMedCrossRefGoogle Scholar
  33. 33.
    Moaven O, Raziee HR, Sima HR, Ganji A, Malekzadeh R, A’Rabi A, Abdollahi A, Memar B, Sotoudeh M, Naseh H, Nekoui N, Razavipour A, Gholamin M, Dadkhah E, Farshchian M, Abbaszadegan MR (2010) Interactions between glutathione-S-transferase m1, t1 and p1 polymorphisms and smoking, and increased susceptibility to esophageal squamous cell carcinoma. Cancer Epidemiol 34:285–290PubMedCrossRefGoogle Scholar
  34. 34.
    Liu R, Yin L, Pu Y, Li Y, Liang G, Zhang J, Li X (2010) Functional alterations in the glutathione S-transferase family associated with enhanced occurrence of esophageal carcinoma in China. J Toxicol Environ Health A 73:471–482PubMedCrossRefGoogle Scholar
  35. 35.
    Ji R, Wu J, Zhou YN, Zhang B, Zhang Z, Yang Z (2010) Relationship between cyp1a1, gstm1 and gstt1 genetic polymorphisms and susceptibility of esophageal cancer in Wuwei, Gansu Province. J Lanzhou Univ 36:29–34Google Scholar
  36. 36.
    Zhang LW, Xia HD, Wu MB, Zhang Z, Li DS, Liu Z (2009) Study on relations between genetic polymorphisms in cyp2c19, gstt1 and risk of Kazakh’s esophageal cancer in Xinjiang. J Pract Oncol 24:232–236Google Scholar
  37. 37.
    Gao P, Qian Y, Ye XF, Ge J, Zhang D, Xu WD (2012) Study of ctpia1, gstt1, gstm1 polymorphisms and susceptibility on esophageal carcinoma in Ningxia Hui nationality. Ningxia Med J 34:196–199Google Scholar
  38. 38.
    Malik MA, Upadhyay R, Mittal RD, Zargar SA, Mittal B (2010) Association of xenobiotic metabolizing enzymes genetic polymorphisms with esophageal cancer in Kashmir valley and influence of environmental factors. Nutr Cancer 62:734–742PubMedCrossRefGoogle Scholar
  39. 39.
    Deng J, Guo RL, Yuen HW, Huang ZG, Ma YX (2008) A case–control study of the polymorphisms of phase I and phase II metabolic genes and esophageal carcinoma susceptibility. Pract J Card Cereb Pneumal Vasc Dis 16:16–18Google Scholar
  40. 40.
    Yi LH, Pu YP, Song YH, Hu X, Liu YZ, Kai HT (2005) Polymorphisms of susceptible genes for esophageal cancer risk in Huaian population in Jiangsu Province. Tumor 25:357–361Google Scholar
  41. 41.
    Abbas A, Delvinquiere K, Lechevrel M, Lebailly P, Gauduchon P, Launoy G, Sichel F (2004) Gstm1, gstt1, gstp1 and cyp1a1 genetic polymorphisms and susceptibility to esophageal cancer in a French population: different pattern of squamous cell carcinoma and adenocarcinoma. World J Gastroenterol 10:3389–3393PubMedGoogle Scholar
  42. 42.
    Wang LD, Zheng S, Liu B, Zhou JX, Li YJ, Li JX (2003) Cyp1a1, gsts and meh polymorphisms and susceptibility to esophageal carcinoma: study of population from a high-incidence area in North China. World J Gastroenterol 9:1394–1397PubMedGoogle Scholar
  43. 43.
    Lin D, Tang Y, Lu S (1998) Glutathione S-transferase m1, t1 genotypes and the risk of esophageal cancer: a case–control study. Zhonghua Liu Xing Bing Xue Za Zhi 19:195–199PubMedGoogle Scholar
  44. 44.
    Lagadu S, Lechevrel M, Sichel F, Breton J, Pottier D, Couderc R, Moussa F, Prevost V (2010) 8-Oxo-7,8-dihydro-2′-deoxyguanosine as a biomarker of oxidative damage in oesophageal cancer patients: lack of association with antioxidant vitamins and polymorphism of hogg1 and gst. J Exp Clin Cancer Res 29:157PubMedCrossRefGoogle Scholar
  45. 45.
    Hatzi VI, Terzoudi GI, Stavropoulou C, Malik SI, Makropoulos V, Pantelias GE (2011) Lack of association between gstt1 polymorphism and endogenous or benzo[a]pyrene-induced sister chromatid exchanges as analyzed in metaphase or g2-phase lymphocytes. Mol Biol Rep 38:3959–3966PubMedCrossRefGoogle Scholar
  46. 46.
    Chen XX, Zhao RP, Qiu LX, Yuan H, Mao C, Hu XC, Guo XM (2011) Glutathione S-transferase t1 polymorphism is associated with breast cancer susceptibility. Cytokine 56:477–480PubMedCrossRefGoogle Scholar
  47. 47.
    Ye Z, Song H, Higgins JP, Pharoah P, Danesh J (2006) Five glutathione S-transferase gene variants in 23,452 cases of lung cancer and 30,397 controls: meta-analysis of 130 studies. PLoS Med 3:e91PubMedCrossRefGoogle Scholar
  48. 48.
    Wlodarczyk M, Nowicka G (2012) Common polymorphisms in cyp1a1, gstm1, gstt1, gstp1 and xpd genes and endogenous DNA damage. Mol Biol Rep 39:5699–5704PubMedCrossRefGoogle Scholar
  49. 49.
    Wang B, Huang G, Wang D, Li A, Xu Z, Dong R, Zhang D, Zhou W (2010) Null genotypes of gstm1 and gstt1 contribute to hepatocellular carcinoma risk: evidence from an updated meta-analysis. J Hepatol 53:508–518PubMedCrossRefGoogle Scholar
  50. 50.
    Bull LM, White DL, Bray M, Nurgalieva Z, El-Serag HB (2009) Phase I and II enzyme polymorphisms as risk factors for Barrett’s esophagus and esophageal adenocarcinoma: a systematic review and meta-analysis. Dis Esophagus 22:571–587PubMedCrossRefGoogle Scholar
  51. 51.
    Moore LE, Baris DR, Figueroa JD, Garcia-Closas M, Karagas MR, Schwenn MR, Johnson AT, Lubin JH, Hein DW, Dagnall CL, Colt JS, Kida M, Jones MA, Schned AR, Cherala SS, Chanock SJ, Cantor KP, Silverman DT, Rothman N (2011) Gstm1 null and nat2 slow acetylation genotypes, smoking intensity and bladder cancer risk: results from the New England bladder cancer study and nat2 meta-analysis. Carcinogenesis 32:182–189PubMedCrossRefGoogle Scholar
  52. 52.
    Zhang ZJ, Hao K, Shi R, Zhao G, Jiang GX, Song Y, Xu X, Ma J (2011) Glutathione S-transferase m1 (gstm1) and glutathione S-transferase t1 (gstt1) null polymorphisms, smoking, and their interaction in oral cancer: a huge review and meta-analysis. Am J Epidemiol 173:847–857PubMedCrossRefGoogle Scholar
  53. 53.
    Piacentini S, Polimanti R, Porreca F, Martinez-Labarga C, De Stefano GF, Fuciarelli M (2011) Gstt1 and gstm1 gene polymorphisms in European and African populations. Mol Biol Rep 38:1225–1230PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Department of Radiation Oncology, Shanghai Pulmonary HospitalTongji University School of MedicineShanghaiChina
  2. 2.Department of Oncology, Shanghai Pulmonary HospitalTongji University School of MedicineShanghaiChina

Personalised recommendations