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Role of GSTT1 Polymorphisms in Cervical Cancer Risk: Influence of Human Papillomavirus Infection and Tobacco Smoke Exposure
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Abstract:
Polymorphisms in certain human genes may contribute to the development of gynecological cancers. While infection with human papillomavirus (HPV) is considered the main cause, studies suggest that deletion of the Glutathione S-Transferase Thêta1 (GSTT1) gene is associated with an increased risk of cervical cancer. The objective of this meta-analysis was to investigate the relationship between GSTT1-null genotype and cervical cancer, and to assess the influence of HPV infection and exposure to tobacco smoke. Our analyses targeted articles published up to June, 13, 2025 in the Web of Science, ScienceDirect, Embase, Scopus, PubMed and Google Scholar databases. We included only case-control studies that evaluated the association between GSTT1 polymorphisms and cervical cancer risk. Summary odds ratios (ORs) with 95% confidence intervals (CIs) were calculated using Meta-Essentials software, applying both fixed-effect model and random-effect models. Subgroup analyses were performed to explore potential sources of heterogeneity and the influence of environmental factors, such as HPV status and tobacco smoke exposure. Thirty-five studies were included in the meta-analyses. Overall, the GSTT1-null genotype was associated with a significantly increased risk of cervical cancer (OR = 1.35; 95%CI = 1.03 - 1.77, p = 0.022) and high-grade intraepithelial lesions (OR = 1.50, 95%CI = 1.15 - 1.96, p = 0.001). In subgroup analysis, significant increased risk was observed, in the pooled subgroup of HPV-positive women (OR = 1.54, 95%CI = 1.09 - 2.16, p = 0.004) and in women exposed to tobacco smoke (OR = 1.31, 95%CI = 1.01 - 1.69, p = 0.019). For high-grade lesions specifically, significant associations were found in Asian populations (OR = 2.23, 95%CI = 1.18 - 4.22, p = 0.000). An association was also observed of HPV-positive infection status. Conversely, no conclusive risk was observed among women not exposed to tobacco smoke and among DNA source (OR < 1 or CI including null value). Altogether, this meta-analysis indicates that the GSTT1-null genotype is associated with a significant increase in the risk of cervical cancer and high-grade.
| [1] | Ferlay, J., Ervik, M., Lam, F., Laversanne, M., Colombet, M., Mery, L., et al. (2024) Global Cancer Observatory: Cancer Today. International Agency for Research on Cancer. |
| [2] | Hausen, H.Z. (1996) Papillomavirus Infections—A Major Cause of Human Cancers. Biochimica et Biophysica Acta (BBA)—Reviews on Cancer, 1288, F55-F78. https://doi.org/10.1016/0304-419x(96)00020-0 |
| [3] | Djigma, F.W., Ouédraogo, C., Karou, D.S., Sagna, T., Bisseye, C., Zeba, M., et al. (2011) Prevalence and Genotype Characterization of Human Papillomaviruses among HIV-Seropositive in Ouagadougou, Burkina Faso. Acta Tropica, 117, 202-206. https://doi.org/10.1016/j.actatropica.2010.12.007 |
| [4] | Ouattara, S., Somé, D.A., Dembélé, A., Sanfo, S., Zohoncon, T., Ouattara, A., et al. (2019) Molecular Epidemiology of High-Risk Human Papilloma Virus Infection in Sexually Active Women at Bobo-Dioulasso University Teaching Hospital. Open Journal of Obstetrics and Gynecology, 9, 1178-1188. https://doi.org/10.4236/ojog.2019.98114 |
| [5] | Ouedraogo, R.A., Zohoncon, T.M., Guigma, S.P., Angèle Traore, I.M., Ouattara, A.K., Ouedraogo, M., et al. (2018) Oncogenic Human Papillomavirus Infection and Genotypes Characterization among Sexually Active Women in Tenkodogo at Burkina Faso, West Africa. Papillomavirus Research, 6, 22-26. https://doi.org/10.1016/j.pvr.2018.09.001 |
| [6] | Zabre, P., Sagna, T., Ouedraogo, R. and Simpore, J. (2024) Epidemiological Profile of Human Papillomavirus Infections and Cervical Cancer Prevention among Sexually Active Women in Burkina Faso: Literature Review. Medical Research Archives, 12, 1-17. https://doi.org/10.18103/mra.v12i11.5883 |
| [7] | Zohoncon, T.M. and Simpore, J. (2013) Prevalence of HPV High-Risk Genotypes in Three Cohorts of Women in Ouagadougou (Burkina Faso). Mediterranean Journal of Hematology and Infectious Diseases, 5, e2013059. https://doi.org/10.4084/mjhid.2013.059 |
| [8] | Hecht, S.S. (1999) Tobacco Smoke Carcinogens and Lung Cancer. JNCI Journal of the National Cancer Institute, 91, 1194-1210. https://doi.org/10.1093/jnci/91.14.1194 |
| [9] | Su, B., Qin, W., Xue, F., Wei, X., Guan, Q., Jiang, W., et al. (2018) The Relation of Passive Smoking with Cervical Cancer: A Systematic Review and Meta-Analysis. Medicine, 97, e13061. https://doi.org/10.1097/md.0000000000013061 |
| [10] | Sugawara, Y., Tsuji, I., Mizoue, T., Inoue, M., Sawada, N., Matsuo, K., et al. (2018) Cigarette Smoking and Cervical Cancer Risk: An Evaluation Based on a Systematic Review and Meta-Analysis among Japanese Women. Japanese Journal of Clinical Oncology, 49, 77-86. https://doi.org/10.1093/jjco/hyy158 |
| [11] | Poppe, W.A.J., Ide, P.S., Drijkoningen, M.P.G., Lauweryns, J.M. and van Assche, A. (1995) Tobacco Smoking Impairs the Local Immunosurveillance in the Uterine Cervix: An Immunohistochemical Study. Gynecologic and Obstetric Investigation, 39, 34-38. https://doi.org/10.1159/000292372 |
| [12] | Giuliano, A.R., Sedjo, R.L., Roe, D.J., Harris, R., Baldwin, S., Papenfuss, M.R., et al. (2002) Clearance of Oncogenic Human Papillomavirus (HPV) Infection: Effect of Smoking (United States). Cancer Causes & Control, 13, 839-846. https://doi.org/10.1023/a:1020668232219 |
| [13] | Koshiol, J., Schroeder, J., Jamieson, D.J., Marshall, S.W., Duerr, A., Heilig, C.M., et al. (2006) Smoking and Time to Clearance of Human Papillomavirus Infection in HIV-Seropositive and HIV-Seronegative Women. American Journal of Epidemiology, 164, 176-183. https://doi.org/10.1093/aje/kwj165 |
| [14] | de Carvalho, C.R.N., da Silva, I.D.C.G., Pereira, J.S., de Souza, N.C.N., Focchi, G.R.A. and Ribalta, J.C.L. (2008) Polymorphisms of p53, GSTM1 and GSTT1, and HPV in Uterine Cervix Adenocarcinoma. European Journal of Gynaecological Oncology, 29, 590-593. |
| [15] | Thakre, T.R., Singh, A. and Mitra, M. (2016) Investigation on Glutathione-S-Transferase M1 and T1 Gene Polymorphisms as Risk Factor in Cervical Cancer. Research Journal of Pharmacy and Technology, 9, 2295-2300. https://doi.org/10.5958/0974-360x.2016.00462.5 |
| [16] | Tacca, A.L.M., Lopes, A.K., Vilanova-Costa, C.A.S.T., Silva, A.M.T.C., Costa, S.H.N., Nogueira, N.A., et al. (2019) Null Polymorphisms in GSTT1 and GSTM1 Genes and Their Associations with Smoking and Cervical Cancer. Genetics and Molecular Research, 18, gmr18067. https://doi.org/10.4238/gmr18067 |
| [17] | Webb, G., Vaska, V., Coggan, M. and Board, P. (1996) Chromosomal Localization of the Gene for the Human Theta Class Glutathione Transferase (GSTT1). Genomics, 33, 121-123. https://doi.org/10.1006/geno.1996.0167 |
| [18] | Schröder, K.R., Wiebel, F.A., Reich, S., Dannappel, D., Bolt, H.M. and Hallier, E. (1995) Glutathione-S-Transferase (GST) Theta Polymorphism Influences Background SCE Rate. Archives of Toxicology, 69, 505-507. https://doi.org/10.1007/s002040050205 |
| [19] | Sadafi, S., Choubsaz, P., Kazemeini, S.M.M., Imani, M.M. and Sadeghi, M. (2024) Glutathione S-Transferase Theta 1 (GSTT1) Deletion Polymorphism and Susceptibility to Head and Neck Carcinoma: A Systematic Review with Five Analyses. BMC Cancer, 24, Article No. 885. https://doi.org/10.1186/s12885-024-12618-7 |
| [20] | Wang, Y., He, J., Ma, T., Lei, W., Li, F., Shen, H., et al. (2016) GSTT1 Null Genotype Significantly Increases the Susceptibility to Urinary System Cancer: Evidences from 63,876 Subjects. Journal of Cancer, 7, 1680-1693. https://doi.org/10.7150/jca.15494 |
| [21] | van Rhee, H., Suurmond, R. and Hak, T. (2015) User Manual for Meta-Essentials: Workbooks for Meta-Analysis. SSRN Electronic Journal, 1-49. https://doi.org/10.2139/ssrn.3241355 |
| [22] | Suurmond, R., van Rhee, H. and Hak, T. (2017) Introduction, Comparison, and Validation of Meta-Essentials: A Free and Simple Tool for Meta-Analysis. Research Synthesis Methods, 8, 537-553. https://doi.org/10.1002/jrsm.1260 |
| [23] | Mantel, N. and Haenszel, W. (1959) Statistical Aspects of the Analysis of Data from Retrospective Studies of Disease. Journal of the National Cancer Institute, 22, 719-748. |
| [24] | DerSimonian, R. and Laird, N. (1986) Meta-Analysis in Clinical Trials. Controlled Clinical Trials, 7, 177-188. https://doi.org/10.1016/0197-2456(86)90046-2 |
| [25] | Schünemann, H.J., Oxman, A.D., Vist, G.E., Higgins, J.P.T.P.T., Deeks, J.J., Glasziou, P., et al. (2011) Confidence Intervals. In: Higgins, J.P.T. and Green, S., Eds., Cochrane Handbook for Systematic Reviews of Interventions (Version 5.1.0) (Section 12), The Cochrane Collaboration. |
| [26] | Cochran, W.G. (1950) The Comparison of Percentages in Matched Samples. Biometrika, 37, 256-266. https://doi.org/10.2307/2332378 |
| [27] | Higgins, J.P.T. and Thompson, S.G. (2002) Quantifying Heterogeneity in a Meta‐analysis. Statistics in Medicine, 21, 1539-1558. https://doi.org/10.1002/sim.1186 |
| [28] | Higgins, J.P.T., Thompson, S.G., Deeks, J.J. and Altman, D.G. (2003) Measuring Inconsistency in Meta-Analyses. BMJ, 327, 557-560. https://doi.org/10.1136/bmj.327.7414.557 |
| [29] | Begg, C.B. and Mazumdar, M. (1994) Operating Characteristics of a Rank Correlation Test for Publication Bias. Biometrics, 50, 1088-1101. https://doi.org/10.2307/2533446 |
| [30] | Egger, M., Smith, G.D., Schneider, M. and Minder, C. (1997) Bias in Meta-Analysis Detected by a Simple, Graphical Test. BMJ, 315, 629-634. https://doi.org/10.1136/bmj.315.7109.629 |
| [31] | Duval, S. and Tweedie, R. (2000) Trim and Fill: A Simple Funnel-Plot-Based Method of Testing and Adjusting for Publication Bias in Meta-Analysis. Biometrics, 56, 455-463. https://doi.org/10.1111/j.0006-341x.2000.00455.x |
| [32] | Duval, S. and Tweedie, R. (2000) A Nonparametric “Trim and Fill” Method of Accounting for Publication Bias in Meta-Analysis. Journal of the American Statistical Association, 95, 89-98. https://doi.org/10.1080/01621459.2000.10473905 |
| [33] | Duval, S. (2005) The Trim and Fill Method. In: Rothstein, H.R., Sutton, A.J. and Borenstein, M., Eds., Publication Bias in Meta-Analysis: Prevention, Assessment and Adjustments, John Wiley & Sons, 127-144. https://doi.org/10.1002/0470870168.ch8 |
| [34] | Liu, C., Zeng, Y., Ma, X., Qi, Y., Zhang, S., Lv, R., et al. (2017) An Updated Meta-Analysis: Cervical Cancer Risk Conferred by GSTM1 and GSTT1 Polymorphisms. International Journal of Sciences, 3, 52-63. https://doi.org/10.18483/ijsci.1179 |
| [35] | Tian, S., Yang, X., Zhang, L., Zhao, J., Pei, M., Yu, Y., et al. (2019) Polymorphic Variants Conferring Genetic Risk to Cervical Lesions Support GSTs as Important Associated Loci. Medicine, 98, e17487. https://doi.org/10.1097/md.0000000000017487 |
| [36] | Thier, R., Wiebel, F.A. and Bolt, H.M. (1999) Differential Substrate Behaviours of Ethylene Oxide and Propylene Oxide Towards Human Glutathione Transferase Theta HGSTT1-1. Archives of Toxicology, 73, 489-492. https://doi.org/10.1007/s002040050640 |
| [37] | Thier, R., Wiebel, F.A., Hinkel, A., Burger, A., Brüning, T., Morgenroth, K., et al. (1998) Species Differences in the Glutathione Transferase GSTT1-1 Activity Towards the Model Substrates Methyl Chloride and Dichloromethane in Liver and Kidney. Archives of Toxicology, 72, 622-629. https://doi.org/10.1007/s002040050552 |
| [38] | Josephy, P.D., Kent, M. and Mannervik, B. (2009) Single-Nucleotide Polymorphic Variants of Human Glutathione Transferase T1-1 Differ in Stability and Functional Properties. Archives of Biochemistry and Biophysics, 490, 24-29. https://doi.org/10.1016/j.abb.2009.07.025 |
| [39] | Moyer, A.M., Sun, Z., Batzler, A.J., Li, L., Schaid, D.J., Yang, P., et al. (2010) Glutathione Pathway Genetic Polymorphisms and Lung Cancer Survival after Platinum-Based Chemotherapy. Cancer Epidemiology, Biomarkers & Prevention, 19, 811-821. https://doi.org/10.1158/1055-9965.epi-09-0871 |
| [40] | Wheeler, H.E., Gamazon, E.R., Stark, A.L., O'Donnell, P.H., Gorsic, L.K., Huang, R.S., et al. (2011) Genome-Wide Meta-Analysis Identifies Variants Associated with Platinating Agent Susceptibility across Populations. The Pharmacogenomics Journal, 13, 35-43. https://doi.org/10.1038/tpj.2011.38 |
| [41] | Thier, R., Pemble, S.E., Kramer, H., Taylor, J.B., Guengerich, F.P. and Ketterer, B. (1996) Short Communication: Human Glutathione S-Transferase T1-1 Enhances Mutagenicity of 1, 2-Dibromoethane, Dibromomethane and 1,2,3,4-Diepoxybutane in salmonella Typhimurium. Carcinogenesis, 17, 163-166. https://doi.org/10.1093/carcin/17.1.163 |
| [42] | Gao, L., Pan, X., Li, L., Liang, W., Bai, P., Rao, L., et al. (2011) Null Genotypes of GSTM1 and GSTT1 Contribute to Risk of Cervical Neoplasia: An Evidence-Based Meta-Analysis. PLOS ONE, 6, e20157. https://doi.org/10.1371/journal.pone.0020157 |
| [43] | Ouedraogo, T.W.C., Djigma, F.W., Idani, B., Zohoncon, T.M., Sorgho, P.A., Bado, P., et al. (2020) Impact of Glutathione S-Transferase Genes Polymorphisms on Human Papillomavirus Infection and Precancerous Lesions in West African Women. |
| [44] | Bortolli, A.P.R., Vieira, V.K., Treco, I.C., Pascotto, C.R., Wendt, G.W. and Lucio, L.C. (2022) GSTT1 and GSTM1 Polymorphisms with Human Papillomavirus Infection in Women from Southern Brazil: A Case-Control Study. Molecular Biology Reports, 49, 6467-6474. https://doi.org/10.1007/s11033-022-07475-1 |
| [45] | Wacholder, S., Silverman, D.T., McLaughlin, J.K. and Mandel, J.S. (1992) Selection of Controls in Case-Control Studies: II. Types of Controls. American Journal of Epidemiology, 135, 1029-1041. https://doi.org/10.1093/oxfordjournals.aje.a116397 |
| [46] | Inácio, Â., Aguiar, L., Rodrigues, B., Pires, P., Ferreira, J., Matos, A., et al. (2023) Genetic Modulation of HPV Infection and Cervical Lesions: Role of Oxidative Stress-Related Genes. Antioxidants, 12, Article 1806. https://doi.org/10.3390/antiox12101806 |
| [47] | Helaoui, A., Sfar, S., Boudhiba, N., Dehghanian, F., Dehbashi, M., Bouchahda, H., et al. (2022) Association of Xenobiotic-Metabolizing Genes Polymorphisms with Cervical Cancer Risk in the Tunisian Population. Molecular Biology Reports, 50, 949-959. https://doi.org/10.1007/s11033-022-07945-6 |
| [48] | Wongpratate, M., Ishida, W., Phuthong, S., Natphopsuk, S. and Ishida, T. (2020) Genetic Polymorphisms of the Human Cytochrome P450 1A1 (CYP1A1) and Cervical Cancer Susceptibility among Northeast Thai Women. Asian Pacific Journal of Cancer Prevention, 21, 243-248. https://doi.org/10.31557/apjcp.2020.21.1.243 |
| [49] | Datkhile, K.D., Patil, M.N., Durgawale, P.P., Korabu, K.S., Joshi, S.A., Gudur, A., et al. (2019) Genetic Polymorphisms in Carcinogen Detoxifying Genes and Risk of Cervical Cancer in Maharashtra, India: A Case Control Study. International Journal of Biomedical Research, 10, e5105. |
| [50] | Phuthong, S., Settheetham-Ishida, W., Natphopsuk, S. and Settheetham, D. (2018) The Correlation between Glutathione S-Transferase Theta-1 (GSTT1) Polymorphism in Relation to Partners’ Smoking and Cervical Cancer Risk. Srinagarind Medical Journal, 33, 107-112. |
| [51] | Satinder, K., Sobti, R.C. and Pushpinder, K. (2017) Impact of Single Nucleotide Polymorphism in Chemical Metabolizing Genes and Exposure to Wood Smoke on Risk of Cervical Cancer in North-Indian Women. Experimental Oncology, 39, 69-74. https://doi.org/10.31768/2312-8852.2017.39(1):69-74 |
| [52] | Sharma, A., Gupta, S., Sodhani, P., Singh, V., Sehgal, A., Sardana, S., et al. (2015) Glutathione S-Transferase M1 and T1 Polymorphisms, Cigarette Smoking and HPV Infection in Precancerous and Cancerous Lesions of the Uterine Cervix. Asian Pacific Journal of Cancer Prevention, 16, 6429-6438. https://doi.org/10.7314/apjcp.2015.16.15.6429 |
| [53] | Nunobiki, O., Ueda, M., Akise, H., Izuma, S., Torii, K., Okamoto, Y., et al. (2015) GSTM1, GSTT1, and NQO1 Polymorphisms in Cervical Carcinogenesis. Human Cell, 28, 109-113. https://doi.org/10.1007/s13577-015-0111-9 |
| [54] | Hasan, S., Hameed, A., Saleem, S., Shahid, S.M., Haider, G. and Azhar, A. (2015) The Association of GSTM1 and GSTT1 Polymorphisms with Squamous Cell Carcinoma of Cervix in Pakistan. Tumor Biology, 36, 5195-5199. https://doi.org/10.1007/s13277-015-3175-y |
| [55] | Stosic, I., Grujicic, D., Arsenijevic, S., Brkic, M. and Milosevic-Djordjevic, O. (2014) Glutathione S-Transferase T1 and M1 Polymorphisms and Risk of Uterine Cervical Lesions in Women from Central Serbia. Asian Pacific Journal of Cancer Prevention, 15, 3201-3205. https://doi.org/10.7314/apjcp.2014.15.7.3201 |
| [56] | De Oliveira Soares, A.J., Bruneska Gondim Martins, D., Perez Bezerra de Medeiros, A.L., De Lima Filho, J.L. and De Araújo, R.F.F. (2013) Association between Glutathione S-Transferase Genotypes, Human Papillomavirus Infection and Development of Cervical Injury in Olinda-Pe. VIRUS Reviews & Research, 18, Article 4. https://doi.org/10.17525/vrrjournal.v18i1-2.66 |
| [57] | Djansugurova, L.B., Perfilyeva, A.V., Zhunusova, G.S., Djantaeva, K.B., Iksan, O.A. and Khussainova, E.M. (2013) The Determination of Genetic Markers of Age-Related Cancer Pathologies in Populations from Kazakhstan. Frontiers in Genetics, 4, Article 70. https://doi.org/10.3389/fgene.2013.00070 |
| [58] | Cseh, J., Pázsit, E., Orsós, Z., Marek, E., Huszár, A., Balogh, S., et al. (2011) Effect of Glutathione-S-Transferase M1 and T1 Allelic Polymorphisms on HPV-Induced Cervical Pre-Cancer Formation. Anticancer Research, 31, 3051-3055. |
| [59] | Nunobiki, O., Ueda, M., Toji, E., Yamamoto, M., Akashi, K., Sato, N., et al. (2011) Genetic Polymorphism of Cancer Susceptibility Genes and HPV Infection in Cervical Carcinogenesis. Pathology Research International, 2011, Article ID: 364069. https://doi.org/10.4061/2011/364069 |
| [60] | Agodi, A., Barchitta, M., Cipresso, R., Marzagalli, R., La Rosa, N., Caruso, M., et al. (2010) Distribution of P53, GST, and MTHFR Polymorphisms and Risk of Cervical Intraepithelial Lesions in Sicily. International Journal of Gynecological Cancer, 20, 141-146. https://doi.org/10.1111/igc.0b013e3181c20842 |
| [61] | Ueda, M., Toji, E., Nunobiki, O., Sato, N., Izuma, S., Torii, K., et al. (2010) Germline Polymorphisms of Glutathione-S-Transferase GSTM1, GSTT1 and P53 Codon 72 in Cervical Carcinogenesis. Human Cell, 23, 119-125. https://doi.org/10.1111/j.1749-0774.2010.00089.x |
| [62] | Kiran, B., Karkucak, M., Ozan, H., Yakut, T., Ozerkan, K., Sag, S., et al. (2010) gst (GSTM1, GSTT1, and GSTP1) Polymorphisms in the Genetic Susceptibility of Turkish Patients to Cervical Cancer. Journal of Gynecologic Oncology, 21, 169-173. https://doi.org/10.3802/jgo.2010.21.3.169 |
| [63] | Palma, S., Novelli, F., Padua, L., Venuti, A., Prignano, G., Mariani, L., et al. (2010) Interaction between Glutathione-S-Transferase Polymorphisms, Smoking Habit, and HPV Infection in Cervical Cancer Risk. Journal of Cancer Research and Clinical Oncology, 136, 1101-1109. https://doi.org/10.1007/s00432-009-0757-3 |
| [64] | Settheetham-Ishida, W., Yuenyao, P., Kularbkaew, C., Settheetham, D. and Ishida, T. (2009) Glutathione S-Transferase (GSTM1 and GSTT1) Polymorphisms in Cervical Cancer in Northeastern Thailand. Asian Pacific Journal of Cancer Prevention, 10, 365-358. |
| [65] | Singh, H., Sachan, R., Devi, S., Pandey, S.N. and Mittal, B. (2008) Association of GSTM1, GSTT1, and GSTM3 Gene Polymorphisms and Susceptibility to Cervical Cancer in a North Indian Population. American Journal of Obstetrics and Gynecology, 198, 303.e1-303.e6. https://doi.org/10.1016/j.ajog.2007.09.046 |
| [66] | Nishino, K., Sekine, M., Kodama, S., Sudo, N., Aoki, Y., Seki, N., et al. (2008) Cigarette Smoking and glutathione S‐transferase M1 Polymorphism Associated with Risk for Uterine Cervical Cancer. Journal of Obstetrics and Gynaecology Research, 34, 994-1001. https://doi.org/10.1111/j.1447-0756.2008.00798.x |
| [67] | Sierra‐Torres, C.H., Arboleda‐Moreno, Y.Y. and Orejuela‐Aristizabal, L. (2006) Exposure to Wood Smoke, HPV Infection, and Genetic Susceptibility for Cervical Neoplasia among Women in Colombia. Environmental and Molecular Mutagenesis, 47, 553-561. https://doi.org/10.1002/em.20228 |
| [68] | Joseph, T., Chacko, P., Wesley, R., Jayaprakash, P.G., James, F.V. and Pillai, M.R. (2006) Germline Genetic Polymorphisms of CYP1A1, GSTM1 and GSTT1 Genes in Indian Cervical Cancer: Associations with Tumor Progression, Age and Human Papillomavirus Infection. Gynecologic Oncology, 101, 411-417. https://doi.org/10.1016/j.ygyno.2005.10.033 |
| [69] | Agorastos, T., Papadopoulos, N., Lambropoulos, A.F., Chrisafi, S., Mikos, T., Goulis, D.G., et al. (2007) Glutathione-S-Transferase M1 and T1 and Cytochrome P1A1 Genetic Polymorphisms and Susceptibility to Cervical Intraepithelial Neoplasia in Greek Women. European Journal of Cancer Prevention, 16, 498-504. https://doi.org/10.1097/01.cej.0000243859.99265.92 |
| [70] | Sobti, R.C., Kaur, S., Kaur, P., Singh, J., Gupta, I., Jain, V., et al. (2006) Interaction of Passive Smoking with GST (GSTM1, GSTT1, and GSTP1) Genotypes in the Risk of Cervical Cancer in India. Cancer Genetics and Cytogenetics, 166, 117-123. https://doi.org/10.1016/j.cancergencyto.2005.10.001 |
| [71] | Niwa, Y., Hirose, K., Nakanishi, T., Nawa, A., Kuzuya, K., Tajima, K., et al. (2005) Association of the NAD(P)H: Quinone Oxidoreductase C609T Polymorphism and the Risk of Cervical Cancer in Japanese Subjects. Gynecologic Oncology, 96, 423-429. https://doi.org/10.1016/j.ygyno.2004.10.015 |
| [72] | Ueda, M., Hung, Y., Terai, Y., Saito, J., Nunobiki, O., Noda, S., et al. (2005) Glutathione-S-Transferase and P53 Polymorphisms in Cervical Carcinogenesis. Gynecologic Oncology, 96, 736-740. https://doi.org/10.1016/j.ygyno.2004.11.005 |
| [73] | Sharma, A., Sharma, J., Murthy, N. and Mitra, A. (2004) Polymorphisms at GSTM1 and GSTT1 Gene Loci and Susceptibility to Cervical Cancer in Indian Population. NEOPLASMA, 51, 12-16. |
| [74] | Lee, S., Kim, J.W., Roh, J.W., Choi, J.Y., Lee, K., Yoo, K., et al. (2004) Genetic Polymorphisms of GSTM1, P21, P53 and HPV Infection with Cervical Cancer in Korean Women. Gynecologic Oncology, 93, 14-18. https://doi.org/10.1016/j.ygyno.2003.11.045 |
| [75] | Goodman, M.T., McDuffie, K., Hernandez, B., Bertram, C.C., Wilkens, L.R., Guo, C., et al. (2001) CYP1A1, GSTM1, and GSTT1 Polymorphisms and the Risk of Cervical Squamous Intraepithelial Lesions in a Multiethnic Population. Gynecologic Oncology, 81, 263-269. https://doi.org/10.1006/gyno.2001.6154 |
| [76] | Kim, J.W., Lee, C.G., Park, Y.G., Kim, K.S., Kim, I., Sohn, Y.W., et al. (2000) Combined Analysis of Germline Polymorphisms of P53, GSTM1, GSTT1, CYP1A1, and CYP2E1: Relation to the Incidence Rate of Cervical Carcinoma. Cancer, 88, 2082-2091. https://doi.org/10.1002/(sici)1097-0142(20000501)88:9<2082::aid-cncr14>3.0.co;2-d |
| [77] | Warwick, A., Sarhanis, P., Redman, C., Pemble, S., Taylor, J.B., Ketterer, B., et al. (1994) Theta Class Glutathione S-Transferase GSTT1 Genotypes and Susceptibility to Cervical Neoplasia: Interactions with GSTM1, CYP2D6 and Smoking. Carcinogenesis, 15, 2841-2845. https://doi.org/10.1093/carcin/15.12.2841 |
