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Published in: Cancer Cell International 1/2019

Open Access 01-12-2019 | Hepatocellular Carcinoma | Primary research

GSTM1 and GSTT1 null genotype increase the risk of hepatocellular carcinoma: evidence based on 46 studies

Authors: Shanli Li, Feng Xue, Yi Zheng, Pengtao Yang, Shuai Lin, Yujiao Deng, Peng Xu, Linghui Zhou, Qian Hao, Zhen Zhai, Ying Wu, Zhijun Dai, Shu Chen

Published in: Cancer Cell International | Issue 1/2019

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Abstract

Background

It is well known that hepatocellular carcinoma (HCC) has been one of the most life-threatening diseases all over the world. Plenty of internal and extrinsic factors have been proven to be related to HCC, such as gene mutation, viral hepatitis, and Nitrosamines. Though previous studies demonstrated that glutathione S-transferase (GST) genotypes are associated with HCC, the conclusions are inconsistent. Therefore, we carried on a renewed meta-analysis to expound the connection between the null GSTM1, GSTT1 polymorphisms and the risk of HCC.

Methods

We searched PubMed, Web of Science, Embase, and CNKI databases to select qualified researches which satisfied the inclusion criteria up to July 31, 2018. Finally, we selected 41 articles with 6124 cases and 9781 controls in this meta-analysis. We use ORs and 95% confidence interval (CI) to evaluate the correlation intension between the GSTM1 and GSTT1 null genes and the risk of HCC. All the statistical processes were executed by Stata (version 12.0).

Results

The pooled analysis showed that both GSTM1 null genotypes (OR = 1.37, 95% CI = 1.18–1.59) and GSTT1 null genotypes (OR = 1.43, 95% CI = 1.23–1.66) increased the risk of HCC. And GSTM1–GSTT1 dual-null genotypes also increased the risk of HCC (OR = 1.58, 95% CI = 1.22–2.05). In the subgroup analysis, we obtained significant results among Asians when stratified by race, and the results are GSTM1 null OR = 1.44, 95% CI = (1.22–1.71), GSTT1 null OR = 1.48, 95% CI = (1.25–1.77), GSTM1–GSTT1 null OR = 1.58, 95% CI = (1.19–2.09), while we didn’t obtain significant results among Caucasians or Africans. Stratified analyses on the type of control indicated a higher risk of HCC associated with GSTM1, GSTT1 single null genotypes and GSTM1–GSTT1 dual-null genotypes in healthy people. No evidence of significant connection was discovered in chronic liver disease (CLD) except in GSTT1 single null.

Conclusions

Our study indicated that an individual who carries the GSTM1, GSTT1 single null genotypes and GSTT1–GSTM1 dual-null genotypes is more likely to develop HCC.
Appendix
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Literature
2.
go back to reference Wei K, Peng X, Liang Z, Cen H. Liver cancer epidemiology world. China Cancer. 2015;24(08):621–30. Wei K, Peng X, Liang Z, Cen H. Liver cancer epidemiology world. China Cancer. 2015;24(08):621–30.
3.
go back to reference Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA: A Cancer J Clin. 2015;65(2):87–108. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA: A Cancer J Clin. 2015;65(2):87–108.
4.
go back to reference Abdel-Rahman O, Helbling D, Schob O, Eltobgy M, Mohamed H, Schmidt J, Giryes A, Mehrabi A, Iype S, John H, et al. Cigarette smoking as a risk factor for the development of and mortality from hepatocellular carcinoma: an updated systematic review of 81 epidemiological studies. J Evid-Based Med. 2017;10(4):245–54.PubMedCrossRef Abdel-Rahman O, Helbling D, Schob O, Eltobgy M, Mohamed H, Schmidt J, Giryes A, Mehrabi A, Iype S, John H, et al. Cigarette smoking as a risk factor for the development of and mortality from hepatocellular carcinoma: an updated systematic review of 81 epidemiological studies. J Evid-Based Med. 2017;10(4):245–54.PubMedCrossRef
5.
go back to reference Yan G, Wang X, Sun C, Zheng X, Wei H, Tian Z, Sun R. Chronic alcohol consumption promotes diethylnitrosamine-induced hepatocarcinogenesis via immune disturbances. Sci Rep. 2017;7(1):2567.PubMedPubMedCentralCrossRef Yan G, Wang X, Sun C, Zheng X, Wei H, Tian Z, Sun R. Chronic alcohol consumption promotes diethylnitrosamine-induced hepatocarcinogenesis via immune disturbances. Sci Rep. 2017;7(1):2567.PubMedPubMedCentralCrossRef
7.
go back to reference Turati F, Edefonti V, Talamini R, Ferraroni M, Malvezzi M, Bravi F, Franceschi S, Montella M, Polesel J, Zucchetto A, et al. Family history of liver cancer and hepatocellular carcinoma. Hepatology. 2012;55(5):1416–25.PubMedCrossRef Turati F, Edefonti V, Talamini R, Ferraroni M, Malvezzi M, Bravi F, Franceschi S, Montella M, Polesel J, Zucchetto A, et al. Family history of liver cancer and hepatocellular carcinoma. Hepatology. 2012;55(5):1416–25.PubMedCrossRef
8.
go back to reference Cheng J, Zhong Y, Chen S, Sun Y, Huang L, Kang Y, Chen B, Chen G, Wang F, Tian Y, et al. Gab2 mediates hepatocellular carcinogenesis by integrating multiple signaling pathways. FASEB J. 2017;31(12):5530–42.PubMedPubMedCentralCrossRef Cheng J, Zhong Y, Chen S, Sun Y, Huang L, Kang Y, Chen B, Chen G, Wang F, Tian Y, et al. Gab2 mediates hepatocellular carcinogenesis by integrating multiple signaling pathways. FASEB J. 2017;31(12):5530–42.PubMedPubMedCentralCrossRef
9.
go back to reference Li R, Boerwinkle E, Olshan AF, Chambless LE, Pankow JS, Tyroler HA, Bray M, Pittman GS, Bell DA, Heiss G. Glutathione S-transferase genotype as a susceptibility factor in smoking-related coronary heart disease. Atherosclerosis. 2000;149(2):451–62.PubMedCrossRef Li R, Boerwinkle E, Olshan AF, Chambless LE, Pankow JS, Tyroler HA, Bray M, Pittman GS, Bell DA, Heiss G. Glutathione S-transferase genotype as a susceptibility factor in smoking-related coronary heart disease. Atherosclerosis. 2000;149(2):451–62.PubMedCrossRef
10.
go back to reference Hayes JD, Strange RC. Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology. 2000;61(3):154–66.PubMedCrossRef Hayes JD, Strange RC. Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology. 2000;61(3):154–66.PubMedCrossRef
12.
go back to reference Dai Z, Feng C, Zhang W, Liu J, Cao X, Zhang H, Liu Y, Wang M, Liu X, Dai Z. Lack of association between cytotoxic T-lymphocyte antigen-4 gene polymorphisms and lymphoid malignancy risk: evidence from a meta-analysis. Ann Hematol. 2016;95(10):1685–94.PubMedCrossRef Dai Z, Feng C, Zhang W, Liu J, Cao X, Zhang H, Liu Y, Wang M, Liu X, Dai Z. Lack of association between cytotoxic T-lymphocyte antigen-4 gene polymorphisms and lymphoid malignancy risk: evidence from a meta-analysis. Ann Hematol. 2016;95(10):1685–94.PubMedCrossRef
13.
go back to reference Zhou L, Zheng Y, Tian T, Liu K, Wang M, Lin S, Deng Y, Dai C, Xu P, Hao Q, et al. Associations of interleukin-6 gene polymorphisms with cancer risk: evidence based on 49,408 cancer cases and 61,790 controls. Gene. 2018;670:136–47.PubMedCrossRef Zhou L, Zheng Y, Tian T, Liu K, Wang M, Lin S, Deng Y, Dai C, Xu P, Hao Q, et al. Associations of interleukin-6 gene polymorphisms with cancer risk: evidence based on 49,408 cancer cases and 61,790 controls. Gene. 2018;670:136–47.PubMedCrossRef
15.
go back to reference Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.PubMed Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.PubMed
16.
go back to reference Imaizumi T, Higaki Y, Hara M, Sakamoto T, Horita M, Mizuta T, Eguchi Y, Yasutake T, Ozaki I, Yamamoto K, et al. Interaction between cytochrome P450 1A2 genetic polymorphism and cigarette smoking on the risk of hepatocellular carcinoma in a Japanese population. Carcinogenesis. 2009;30(10):1729–34.PubMedCrossRef Imaizumi T, Higaki Y, Hara M, Sakamoto T, Horita M, Mizuta T, Eguchi Y, Yasutake T, Ozaki I, Yamamoto K, et al. Interaction between cytochrome P450 1A2 genetic polymorphism and cigarette smoking on the risk of hepatocellular carcinoma in a Japanese population. Carcinogenesis. 2009;30(10):1729–34.PubMedCrossRef
17.
go back to reference Kiran M, Chawla YK, Kaur J. Glutathione-S-transferase and microsomal epoxide hydrolase polymorphism and viral-related hepatocellular carcinoma risk in India. DNA Cell Biol. 2008;27(12):687–94.PubMedCrossRef Kiran M, Chawla YK, Kaur J. Glutathione-S-transferase and microsomal epoxide hydrolase polymorphism and viral-related hepatocellular carcinoma risk in India. DNA Cell Biol. 2008;27(12):687–94.PubMedCrossRef
18.
go back to reference Zhang Y, Deng C, Zhu Y. Study on genetic polymorphisms of xenobiotic metabolizing enzymes in hepatitis B virus-associated hepatic diseases. J Wenzhou Med Coll. 2005;35(06):464–7. Zhang Y, Deng C, Zhu Y. Study on genetic polymorphisms of xenobiotic metabolizing enzymes in hepatitis B virus-associated hepatic diseases. J Wenzhou Med Coll. 2005;35(06):464–7.
19.
go back to reference Deng Z, Wei Y, Ma Y. Genetic deletion of GSTM1 and GSTT1 detoxicated enzymes in relation to hepatocellular carcinoma in Guangxi. Guangxi Sciences. 2005;12(01):55–7. Deng Z, Wei Y, Ma Y. Genetic deletion of GSTM1 and GSTT1 detoxicated enzymes in relation to hepatocellular carcinoma in Guangxi. Guangxi Sciences. 2005;12(01):55–7.
20.
go back to reference Zhu M, Chen X, Zhou L. Association of genetic polymorphisms in glutathione S-transferases M1 with hepatitis B-related hepatocellular carcinoma. J Zhejiang Univ. 2005;34(02):35–9. Zhu M, Chen X, Zhou L. Association of genetic polymorphisms in glutathione S-transferases M1 with hepatitis B-related hepatocellular carcinoma. J Zhejiang Univ. 2005;34(02):35–9.
21.
go back to reference Boccia S, Miele L, Panic N. The effect of CYP GST, and SULT polymorphisms and their interaction with smoking on the risk of hepatocellular carcinoma. Biomed Res Int. 2015;2015:179867.PubMedPubMedCentral Boccia S, Miele L, Panic N. The effect of CYP GST, and SULT polymorphisms and their interaction with smoking on the risk of hepatocellular carcinoma. Biomed Res Int. 2015;2015:179867.PubMedPubMedCentral
22.
go back to reference Chen Y, Ding F, Xie Y-A. Study on gene polymorphisms of glutathione S-transferase GSTM1 and GSTT1 in high-risk families for liver cancer in Fusui county, Guangxi. Chin J of Oncol Prev and Treat. 2012;4(02):140–4. Chen Y, Ding F, Xie Y-A. Study on gene polymorphisms of glutathione S-transferase GSTM1 and GSTT1 in high-risk families for liver cancer in Fusui county, Guangxi. Chin J of Oncol Prev and Treat. 2012;4(02):140–4.
23.
go back to reference Tang Y, Li X, Liu T. A study of genetic polymorphisms of glutathione S-transferase in patients with hepatocellular carcinoma. Chin J Lab Diagn. 2012, 16(04):660–2. Tang Y, Li X, Liu T. A study of genetic polymorphisms of glutathione S-transferase in patients with hepatocellular carcinoma. Chin J Lab Diagn. 2012, 16(04):660–2.
24.
go back to reference Li CG, Zhao ZM, Hu MG, Liu R. Predictive role of glutathione-S-transferase gene polymorphisms in risk and prognosis of hepatocellular carcinoma. Asian Pac J Cancer Prev APJCP. 2012;13(7):3247–52.PubMedCrossRef Li CG, Zhao ZM, Hu MG, Liu R. Predictive role of glutathione-S-transferase gene polymorphisms in risk and prognosis of hepatocellular carcinoma. Asian Pac J Cancer Prev APJCP. 2012;13(7):3247–52.PubMedCrossRef
25.
go back to reference Sarma MP, Asim M, Medhi S, Bharathi T, Kar P. Hepatitis C virus related hepatocellular carcinoma: a case control study from India. J Med Virol. 2012;84(7):1009–17.PubMedCrossRef Sarma MP, Asim M, Medhi S, Bharathi T, Kar P. Hepatitis C virus related hepatocellular carcinoma: a case control study from India. J Med Virol. 2012;84(7):1009–17.PubMedCrossRef
26.
go back to reference Xiao K, Li L, Peng M, Qin X, Peng T, Guo Y. Gene polymorphisms of GSTM1 and GSTT1 in the clustering families of hepatocellular carcinoma. Chin J Oncol Prev Treat. 2011;3(04):287–90. Xiao K, Li L, Peng M, Qin X, Peng T, Guo Y. Gene polymorphisms of GSTM1 and GSTT1 in the clustering families of hepatocellular carcinoma. Chin J Oncol Prev Treat. 2011;3(04):287–90.
27.
go back to reference Wei Y, Long X, Liu Z, Ma Y, Deng Z. Genetic polymorphism of glutathione-S-transferase M1 and T1 in hepatocellular carcinoma and nasopharyngeal carcinoma. Cancer Prev Res. 2010;37(10):1162–5. Wei Y, Long X, Liu Z, Ma Y, Deng Z. Genetic polymorphism of glutathione-S-transferase M1 and T1 in hepatocellular carcinoma and nasopharyngeal carcinoma. Cancer Prev Res. 2010;37(10):1162–5.
28.
go back to reference Kao CC, Chen MK, Kuo WH, Chen TY, Su SC, Hsieh YH, Liu CL, Chou MC, Tsai HT, Yang SF. Influence of glutathione-S-transferase theta (GSTT1) and micro (GSTM1) gene polymorphisms on the susceptibility of hepatocellular carcinoma in Taiwan. J Surg Oncol. 2010;102(4):301–7.PubMedCrossRef Kao CC, Chen MK, Kuo WH, Chen TY, Su SC, Hsieh YH, Liu CL, Chou MC, Tsai HT, Yang SF. Influence of glutathione-S-transferase theta (GSTT1) and micro (GSTM1) gene polymorphisms on the susceptibility of hepatocellular carcinoma in Taiwan. J Surg Oncol. 2010;102(4):301–7.PubMedCrossRef
29.
go back to reference Asim M, Khan LA, Husain SA, Husain S, Sarma MP, Ahmad I, Sharma JK, Sharma A, Sharma S, Thayumanavan L, et al. Genetic polymorphism of glutathione S transferases M1 and T1 in Indian patients with hepatocellular carcinoma. Dis Markers. 2010;28(6):369–76.PubMedPubMedCentralCrossRef Asim M, Khan LA, Husain SA, Husain S, Sarma MP, Ahmad I, Sharma JK, Sharma A, Sharma S, Thayumanavan L, et al. Genetic polymorphism of glutathione S transferases M1 and T1 in Indian patients with hepatocellular carcinoma. Dis Markers. 2010;28(6):369–76.PubMedPubMedCentralCrossRef
30.
go back to reference Yang Z, Xie Y-A, Kuang Z, Luo X, Zhang W, Leng C. Relationship between genetic polymorphisms of glutathione-S-transferase M1, T1 genes and susceptibility to hepatocellular carcinoma in population of Fusui District of Guangxi Zhuang Autonomous Region. Chin J Caner Prev Treat. 2009;16(13):970–3. Yang Z, Xie Y-A, Kuang Z, Luo X, Zhang W, Leng C. Relationship between genetic polymorphisms of glutathione-S-transferase M1, T1 genes and susceptibility to hepatocellular carcinoma in population of Fusui District of Guangxi Zhuang Autonomous Region. Chin J Caner Prev Treat. 2009;16(13):970–3.
31.
go back to reference He S, Gu Y, Liao Z. Relationship between GSTM1 gene polymorphism, tobacco and alcohol habits and susceptibility to primary liver cancer. J Guangxi Medi Univ. 2008;25(04):567–8. He S, Gu Y, Liao Z. Relationship between GSTM1 gene polymorphism, tobacco and alcohol habits and susceptibility to primary liver cancer. J Guangxi Medi Univ. 2008;25(04):567–8.
32.
go back to reference Abd El-Moneim E, Younis FA, Allam N, Gameel K, Osman M. Gene deletion of glutathione S-transferase M1 and T1 and risk factors of hepatocellular carcinoma in Egyptian patients. Egypt J Immunol. 2008;15(2):125–34.PubMed Abd El-Moneim E, Younis FA, Allam N, Gameel K, Osman M. Gene deletion of glutathione S-transferase M1 and T1 and risk factors of hepatocellular carcinoma in Egyptian patients. Egypt J Immunol. 2008;15(2):125–34.PubMed
33.
go back to reference Borentain P, Gerolami V, Ananian P, Garcia S, Noundou A, Botta-Fridlund D, Le Treut YP, Berge-Lefranc JL, Gerolami R. DNA-repair and carcinogen-metabolising enzymes genetic polymorphisms as an independent risk factor for hepatocellular carcinoma in Caucasian liver-transplanted patients. Eur J Cancer. 2007;43(17):2479–86.PubMedCrossRef Borentain P, Gerolami V, Ananian P, Garcia S, Noundou A, Botta-Fridlund D, Le Treut YP, Berge-Lefranc JL, Gerolami R. DNA-repair and carcinogen-metabolising enzymes genetic polymorphisms as an independent risk factor for hepatocellular carcinoma in Caucasian liver-transplanted patients. Eur J Cancer. 2007;43(17):2479–86.PubMedCrossRef
34.
go back to reference Deng W. The study of correlation between the polymorphism of GST genes and familial susceptibility to hepatocellular carcinoma in the high incidence area of Guangxi. Master: Guangxi Medical University; 2006. Deng W. The study of correlation between the polymorphism of GST genes and familial susceptibility to hepatocellular carcinoma in the high incidence area of Guangxi. Master: Guangxi Medical University; 2006.
35.
go back to reference Long XD, Ma Y, Wei YP, Deng ZL. The polymorphisms of GSTM1, GSTT1, HYL1*2, and XRCC1, and aflatoxin B1-related hepatocellular carcinoma in Guangxi population, China. Hepatol Res. 2006;36(1):48–55.PubMedCrossRef Long XD, Ma Y, Wei YP, Deng ZL. The polymorphisms of GSTM1, GSTT1, HYL1*2, and XRCC1, and aflatoxin B1-related hepatocellular carcinoma in Guangxi population, China. Hepatol Res. 2006;36(1):48–55.PubMedCrossRef
36.
go back to reference Ladero JM, Martinez C, Garcia-Martin E, Ropero P, Briceno O, Villegas A, Diaz-Rubio M, Agundez JA. Glutathione S-transferase M1 and T1 genetic polymorphisms are not related to the risk of hepatocellular carcinoma: a study in the Spanish population. Eur J Cancer. 2006;42(1):73–7.PubMedCrossRef Ladero JM, Martinez C, Garcia-Martin E, Ropero P, Briceno O, Villegas A, Diaz-Rubio M, Agundez JA. Glutathione S-transferase M1 and T1 genetic polymorphisms are not related to the risk of hepatocellular carcinoma: a study in the Spanish population. Eur J Cancer. 2006;42(1):73–7.PubMedCrossRef
37.
go back to reference Guo H, Bian J, Jiang F, Wang Q, Zhang Z, Fan W, Wang Q, Zhu X, Tang B. The null genotypes ofGSTM1 and GSTT1 and the genetic susceptibility of prmiary liver cancer in Luoyang, China. Tumor. 2005;25(01):58–61. Guo H, Bian J, Jiang F, Wang Q, Zhang Z, Fan W, Wang Q, Zhu X, Tang B. The null genotypes ofGSTM1 and GSTT1 and the genetic susceptibility of prmiary liver cancer in Luoyang, China. Tumor. 2005;25(01):58–61.
38.
go back to reference Long X, Ma Y, Wei Y, Deng Z. A study about the association of detoxication gene GSTM1 polymorphism and the susceptibility to aflatoxin B1-related hepatocellular carcinoma. Chin J Hepatol. 2005;13(09):668–70. Long X, Ma Y, Wei Y, Deng Z. A study about the association of detoxication gene GSTM1 polymorphism and the susceptibility to aflatoxin B1-related hepatocellular carcinoma. Chin J Hepatol. 2005;13(09):668–70.
39.
go back to reference He S, Qin J, Gu Y, Zhong W, Su S. Polymorphism analysis of GSTM1 and GSTT1 genes in patients with hepatocellular carcinoma. J Guangxi Med Univ. 2005;22(06):875–7. He S, Qin J, Gu Y, Zhong W, Su S. Polymorphism analysis of GSTM1 and GSTT1 genes in patients with hepatocellular carcinoma. J Guangxi Med Univ. 2005;22(06):875–7.
40.
go back to reference Gelatti U, Covolo L, Talamini R, Tagger A, Barbone F, Martelli C, Cremaschini F, Franceschi S, Ribero ML, Garte S, et al. N-Acetyltransferase-2, glutathione S-transferase M1 and T1 genetic polymorphisms, cigarette smoking and hepatocellular carcinoma: a case-control study. Int J Cancer. 2005;115(2):301–6.PubMedCrossRef Gelatti U, Covolo L, Talamini R, Tagger A, Barbone F, Martelli C, Cremaschini F, Franceschi S, Ribero ML, Garte S, et al. N-Acetyltransferase-2, glutathione S-transferase M1 and T1 genetic polymorphisms, cigarette smoking and hepatocellular carcinoma: a case-control study. Int J Cancer. 2005;115(2):301–6.PubMedCrossRef
41.
go back to reference Kirk GD, Turner PC, Gong Y, Lesi OA, Mendy M, Goedert JJ, Hall AJ, Whittle H, Hainaut P, Montesano R, et al. Hepatocellular carcinoma and polymorphisms in carcinogen-metabolizing and DNA repair enzymes in a population with aflatoxin exposure and hepatitis B virus endemicity. Cancer Epidemiol Biomarkers Prev. 2005;14(2):373–9.PubMedCrossRef Kirk GD, Turner PC, Gong Y, Lesi OA, Mendy M, Goedert JJ, Hall AJ, Whittle H, Hainaut P, Montesano R, et al. Hepatocellular carcinoma and polymorphisms in carcinogen-metabolizing and DNA repair enzymes in a population with aflatoxin exposure and hepatitis B virus endemicity. Cancer Epidemiol Biomarkers Prev. 2005;14(2):373–9.PubMedCrossRef
42.
go back to reference Ma D, Chen Y, Li Y, Zhao H, Xie X, Lu X. Glutathione-S-transferase M1 and T1 polymorphisms and susceptibility to liver cancer in hepatitis B surface antigen positive population. Med J Chin People’ s Armed Police Forces. 2005;16(09):660–2. Ma D, Chen Y, Li Y, Zhao H, Xie X, Lu X. Glutathione-S-transferase M1 and T1 polymorphisms and susceptibility to liver cancer in hepatitis B surface antigen positive population. Med J Chin People’ s Armed Police Forces. 2005;16(09):660–2.
43.
go back to reference Li S, Wu J, Ding J, Gao C, Cao H, Zhou X. Impact of Genetic polymorphisms of glutathione S-transferase T1, M1 on the risk of primary hepatocellular carcinoma in alcohol drinkers. Pract J Cancer. 2004;19(03):229–32. Li S, Wu J, Ding J, Gao C, Cao H, Zhou X. Impact of Genetic polymorphisms of glutathione S-transferase T1, M1 on the risk of primary hepatocellular carcinoma in alcohol drinkers. Pract J Cancer. 2004;19(03):229–32.
44.
go back to reference Yu MW, Yang SY, Pan IJ, Lin CL, Liu CJ, Liaw YF, Lin SM, Chen PJ, Lee SD, Chen CJ. Polymorphisms in XRCC1 and glutathione S-transferase genes and hepatitis B-related hepatocellular carcinoma. J Natl Cancer Inst. 2003;95(19):1485–8.PubMedCrossRef Yu MW, Yang SY, Pan IJ, Lin CL, Liu CJ, Liaw YF, Lin SM, Chen PJ, Lee SD, Chen CJ. Polymorphisms in XRCC1 and glutathione S-transferase genes and hepatitis B-related hepatocellular carcinoma. J Natl Cancer Inst. 2003;95(19):1485–8.PubMedCrossRef
45.
go back to reference Liu Z. Genetic polymorphism of GSTT1 and EPHX and the risk of Hepatocellular carcinoma from Guangxi district. Master: Guangxi Med Univ; 2003. Liu Z. Genetic polymorphism of GSTT1 and EPHX and the risk of Hepatocellular carcinoma from Guangxi district. Master: Guangxi Med Univ; 2003.
46.
go back to reference Munaka M, Kohshi K, Kawamoto T, Takasawa S, Nagata N, Itoh H, Oda S, Katoh T. Genetic polymorphisms of tobacco- and alcohol-related metabolizing enzymes and the risk of hepatocellular carcinoma. J Cancer Res Clin Oncol. 2003;129(6):355–60.PubMedCrossRef Munaka M, Kohshi K, Kawamoto T, Takasawa S, Nagata N, Itoh H, Oda S, Katoh T. Genetic polymorphisms of tobacco- and alcohol-related metabolizing enzymes and the risk of hepatocellular carcinoma. J Cancer Res Clin Oncol. 2003;129(6):355–60.PubMedCrossRef
47.
go back to reference Chen SY, Wang LY, Lunn RM, Tsai WY, Lee PH, Lee CS, Ahsan H, Zhang YJ, Chen CJ, Santella RM. Polycyclic aromatic hydrocarbon-DNA adducts in liver tissues of hepatocellular carcinoma patients and controls. Int J Cancer. 2002;99(1):14–21.PubMedCrossRef Chen SY, Wang LY, Lunn RM, Tsai WY, Lee PH, Lee CS, Ahsan H, Zhang YJ, Chen CJ, Santella RM. Polycyclic aromatic hydrocarbon-DNA adducts in liver tissues of hepatocellular carcinoma patients and controls. Int J Cancer. 2002;99(1):14–21.PubMedCrossRef
48.
go back to reference Tiemersma EW, Omer RE, Bunschoten A, van’t Veer P, Kok FJ, Idris MO, Kadaru AM, Fedail SS, Kampman E. Role of genetic polymorphism of glutathione-S-transferase T1 and microsomal epoxide hydrolase in aflatoxin-associated hepatocellular carcinoma. Cancer Epidemiol Biomarkers Prev. 2001;10(7):785–91.PubMed Tiemersma EW, Omer RE, Bunschoten A, van’t Veer P, Kok FJ, Idris MO, Kadaru AM, Fedail SS, Kampman E. Role of genetic polymorphism of glutathione-S-transferase T1 and microsomal epoxide hydrolase in aflatoxin-associated hepatocellular carcinoma. Cancer Epidemiol Biomarkers Prev. 2001;10(7):785–91.PubMed
49.
go back to reference Sun CA, Wang LY, Chen CJ, Lu SN, You SL, Wang LW, Wang Q, Wu DM, Santella RM. Genetic polymorphisms of glutathione S-transferases M1 and T1 associated with susceptibility to aflatoxin-related hepatocarcinogenesis among chronic hepatitis B carriers: a nested case–control study in Taiwan. Carcinogenesis. 2001;22(8):1289–94.PubMedCrossRef Sun CA, Wang LY, Chen CJ, Lu SN, You SL, Wang LW, Wang Q, Wu DM, Santella RM. Genetic polymorphisms of glutathione S-transferases M1 and T1 associated with susceptibility to aflatoxin-related hepatocarcinogenesis among chronic hepatitis B carriers: a nested case–control study in Taiwan. Carcinogenesis. 2001;22(8):1289–94.PubMedCrossRef
50.
go back to reference Zhu W, Chen Q, Luo C, Chu X, Wu M. Relationship study between gene polymorphism of CYP1A1, GSTM1 and genetic susceptibility of primary hepatocellar carcinoma. China J Cancer Prev Treat. 2001;8(06):572–4. Zhu W, Chen Q, Luo C, Chu X, Wu M. Relationship study between gene polymorphism of CYP1A1, GSTM1 and genetic susceptibility of primary hepatocellar carcinoma. China J Cancer Prev Treat. 2001;8(06):572–4.
51.
go back to reference Bian JC, Shen FM, Shen L, Wang TR, Wang XH, Chen GC, Wang JB. Susceptibility to hepatocellular carcinoma associated with null genotypes of GSTM1 and GSTT1. World J Gastroenterol. 2000;6(2):228–30.PubMedPubMedCentral Bian JC, Shen FM, Shen L, Wang TR, Wang XH, Chen GC, Wang JB. Susceptibility to hepatocellular carcinoma associated with null genotypes of GSTM1 and GSTT1. World J Gastroenterol. 2000;6(2):228–30.PubMedPubMedCentral
52.
go back to reference Wu H, Chen M, Liu P, Zhang R. Relationship between GSTM1 gene polymorphism and genet ic susceptibility to primary hepatocellular carcinoma. Pract J Cancer. 2000;15(05):463–5. Wu H, Chen M, Liu P, Zhang R. Relationship between GSTM1 gene polymorphism and genet ic susceptibility to primary hepatocellular carcinoma. Pract J Cancer. 2000;15(05):463–5.
53.
go back to reference Yu MW, Chiu YH, Chiang YC, Chen CH, Lee TH, Santella RM, Chern HD, Liaw YF, Chen CJ. Plasma carotenoids, glutathione S-transferase M1 and T1 genetic polymorphisms, and risk of hepatocellular carcinoma: independent and interactive effects. Am J Epidemiol. 1999;149(7):621–9.PubMedCrossRef Yu MW, Chiu YH, Chiang YC, Chen CH, Lee TH, Santella RM, Chern HD, Liaw YF, Chen CJ. Plasma carotenoids, glutathione S-transferase M1 and T1 genetic polymorphisms, and risk of hepatocellular carcinoma: independent and interactive effects. Am J Epidemiol. 1999;149(7):621–9.PubMedCrossRef
54.
go back to reference Dong C, Zi X, Yu S, Han J. Relationship between deletion of slutathion S-trausferase gene and susceptibility to primary hepatocellular carcinoma. Chin J Public Health. 1997;16(03):15–6. Dong C, Zi X, Yu S, Han J. Relationship between deletion of slutathion S-trausferase gene and susceptibility to primary hepatocellular carcinoma. Chin J Public Health. 1997;16(03):15–6.
55.
go back to reference Dong C, Yu S, Chen G, Deming Z, Fu Y. Polymorphisms of GSTT1 and M1 genotypes and their effects on elevated aflatoxin exposure and increased risk of hepatocellular carcinoma. Cancer Prev Res. 1997;24(06):327–9. Dong C, Yu S, Chen G, Deming Z, Fu Y. Polymorphisms of GSTT1 and M1 genotypes and their effects on elevated aflatoxin exposure and increased risk of hepatocellular carcinoma. Cancer Prev Res. 1997;24(06):327–9.
56.
go back to reference Yu MW, Gladek-Yarborough A, Chiamprasert S, Santella RM, Liaw YF, Chen CJ. Cytochrome P450 2E1 and glutathione S-transferase M1 polymorphisms and susceptibility to hepatocellular carcinoma. Gastroenterology. 1995;109(4):1266–73.PubMedCrossRef Yu MW, Gladek-Yarborough A, Chiamprasert S, Santella RM, Liaw YF, Chen CJ. Cytochrome P450 2E1 and glutathione S-transferase M1 polymorphisms and susceptibility to hepatocellular carcinoma. Gastroenterology. 1995;109(4):1266–73.PubMedCrossRef
57.
go back to reference Wang ZY, Zhou J, Luo L, Huang YL, Dong PD. Predictive role of glutathione-S-transferase gene polymorphisms in the survival of gastric cancer cases. Asian Pac J Cancer Prev: APJCP. 2012;13(4):1515–8.PubMedCrossRef Wang ZY, Zhou J, Luo L, Huang YL, Dong PD. Predictive role of glutathione-S-transferase gene polymorphisms in the survival of gastric cancer cases. Asian Pac J Cancer Prev: APJCP. 2012;13(4):1515–8.PubMedCrossRef
58.
go back to reference Coric VM, Simic TP, Pekmezovic TD, Basta-Jovanovic GM, Savic-Radojevic AR, Radojevic-Skodric SM, Matic MG, Suvakov SR, Dragicevic DP, Radic TM, et al. GSTM1 genotype is an independent prognostic factor in clear cell renal cell carcinoma. Urol Oncol. 2017;35(6):409–17.PubMedCrossRef Coric VM, Simic TP, Pekmezovic TD, Basta-Jovanovic GM, Savic-Radojevic AR, Radojevic-Skodric SM, Matic MG, Suvakov SR, Dragicevic DP, Radic TM, et al. GSTM1 genotype is an independent prognostic factor in clear cell renal cell carcinoma. Urol Oncol. 2017;35(6):409–17.PubMedCrossRef
59.
go back to reference Sharma N, Singh A, Singh N, Behera D, Sharma S. Genetic polymorphisms in GSTM1, GSTT1 and GSTP1 genes and risk of lung cancer in a North Indian population. Cancer Epidemiol. 2015;39(6):947–55.PubMedCrossRef Sharma N, Singh A, Singh N, Behera D, Sharma S. Genetic polymorphisms in GSTM1, GSTT1 and GSTP1 genes and risk of lung cancer in a North Indian population. Cancer Epidemiol. 2015;39(6):947–55.PubMedCrossRef
60.
go back to reference White DL, Li D, Nurgalieva Z, El-Serag HB. Genetic variants of glutathione S-transferase as possible risk factors for hepatocellular carcinoma: a HuGE systematic review and meta-analysis. Am J Epidemiol. 2008;167(4):377–89.PubMedCrossRef White DL, Li D, Nurgalieva Z, El-Serag HB. Genetic variants of glutathione S-transferase as possible risk factors for hepatocellular carcinoma: a HuGE systematic review and meta-analysis. Am J Epidemiol. 2008;167(4):377–89.PubMedCrossRef
61.
go back to reference Song K, Yi J, Shen X, Cai Y. Genetic polymorphisms of glutathione S-transferase genes GSTM1, GSTT1 and risk of hepatocellular carcinoma. PLoS ONE. 2012;7(11):e48924.PubMedPubMedCentralCrossRef Song K, Yi J, Shen X, Cai Y. Genetic polymorphisms of glutathione S-transferase genes GSTM1, GSTT1 and risk of hepatocellular carcinoma. PLoS ONE. 2012;7(11):e48924.PubMedPubMedCentralCrossRef
62.
go back to reference Shen YH, Chen S, Peng YF, Shi YH, Huang XW, Yang GH, Ding ZB, Yi Y, Zhou J, Qiu SJ, et al. Quantitative assessment of the effect of glutathione S-transferase genes GSTM1 and GSTT1 on hepatocellular carcinoma risk. Tumour Biol. 2014;35(5):4007–15.PubMedCrossRef Shen YH, Chen S, Peng YF, Shi YH, Huang XW, Yang GH, Ding ZB, Yi Y, Zhou J, Qiu SJ, et al. Quantitative assessment of the effect of glutathione S-transferase genes GSTM1 and GSTT1 on hepatocellular carcinoma risk. Tumour Biol. 2014;35(5):4007–15.PubMedCrossRef
63.
go back to reference Yuan BH, Li RH, Yuan WP, Xiang BD, Zheng MH, Yang T, Zhong JH, Li LQ. Perioperative entecavir for patients with HBV-related hepatocellular carcinoma and low levels of viral DNA: analysis using propensity score matching. Oncotarget. 2017;8(31):51810–6.PubMedPubMedCentralCrossRef Yuan BH, Li RH, Yuan WP, Xiang BD, Zheng MH, Yang T, Zhong JH, Li LQ. Perioperative entecavir for patients with HBV-related hepatocellular carcinoma and low levels of viral DNA: analysis using propensity score matching. Oncotarget. 2017;8(31):51810–6.PubMedPubMedCentralCrossRef
64.
go back to reference Chu YJ, Yang HI, Wu HC, Liu J, Wang LY, Lu SN, Lee MH, Jen CL, You SL, Santella RM, et al. Aflatoxin B1 exposure increases the risk of cirrhosis and hepatocellular carcinoma in chronic hepatitis B virus carriers. Int J Cancer. 2017;141(4):711–20.PubMedPubMedCentralCrossRef Chu YJ, Yang HI, Wu HC, Liu J, Wang LY, Lu SN, Lee MH, Jen CL, You SL, Santella RM, et al. Aflatoxin B1 exposure increases the risk of cirrhosis and hepatocellular carcinoma in chronic hepatitis B virus carriers. Int J Cancer. 2017;141(4):711–20.PubMedPubMedCentralCrossRef
65.
go back to reference Gao SS, Chen XY, Zhu RZ, Choi BM, Kim SJ, Kim BR. Dual effects of phloretin on aflatoxin B1 metabolism: activation and detoxification of aflatoxin B1. BioFactors. 2012;38(1):34–43.PubMedCrossRef Gao SS, Chen XY, Zhu RZ, Choi BM, Kim SJ, Kim BR. Dual effects of phloretin on aflatoxin B1 metabolism: activation and detoxification of aflatoxin B1. BioFactors. 2012;38(1):34–43.PubMedCrossRef
Metadata
Title
GSTM1 and GSTT1 null genotype increase the risk of hepatocellular carcinoma: evidence based on 46 studies
Authors
Shanli Li
Feng Xue
Yi Zheng
Pengtao Yang
Shuai Lin
Yujiao Deng
Peng Xu
Linghui Zhou
Qian Hao
Zhen Zhai
Ying Wu
Zhijun Dai
Shu Chen
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2019
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-019-0792-3

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