Relationship between the Polymorphism of the GSTP1 (rs1695) Gene and Chronic Hepatitis B Infection in Ouagadougou, Burkina Faso

Tilate Lare¹, Lassina Traore¹, Marie Simone Traore², Sidnooma Véronique Zongo¹, Pierre Zabre¹, Mousso Savadogo¹, Fortune D. Salah³, Herman Karim Sombie⁴, Pegdwendé Abel Sorgho^1,4, Tégwindé Rebeca Compaore⁵, Tani Sagna⁵, Issoufou Tao⁶, Florencia Wendkuuni Djigma^1*, Dorcas Obiri-Yeboah⁷, Damintoti Simplice Karou⁸, Rogomenoma Alice Ouedraogo⁹, Teega-Wende Clarisse Ouedraogo¹, Prosper Bado⁴, Albert Théophane Yonli⁴, Jacques Simpore^1,4

¹Laboratoire de Biologie Moléculaire et de Génétique, Université Joseph KI-ZERBO, Ouagadougou, Burkina Faso.
²Ecole Normale Supérieure, Ouagadougou, Burkina Faso.
³Laboratoire de Biologie Moléculaire-Virologie, Institut National d’Hygiène, Lomé, Togo.
⁴Centre de Recherche Biomoléculaire Pietro Annigoni (CERBA), Ouagadougou, Burkina Faso.
⁵Centre National de la Recherche Scientifique et Technologique, Institut de Recherche en Sciences de la Santé, Ouagadougou, Burkina Faso.
⁶Institut des Sciences et de Technologies/Ecole Normale Supérieure, Koudougou, Burkina Faso.
⁷Department of Microbiology and Immunology, School of Medical Sciences, University of Cape Coast, PMB, Cape Coast, Ghana.
⁸école Supérieure des Techniques Biologiques et Alimentaires, Université de Lomé (ESTBA-UL), Lomé, Togo.
⁹Centre Universitaire de Gaoua, Université Nazi Boni, Bobo-Dioulasso, Burkina Faso.

DOI: 10.4236/jbm.2023.1111009                

Abstract

Introduction: Genetic polymorphisms of some Glutathione S-Transferase (GST) which encode the enzyme responsible for the biotransformation of drugs and xenobiotics, have been associated with the risk of several pathologies that can progress to cancer such as Hepatitis B. This study aims to characterize the impact of the rs1695 polymorphism of GSTP1 gene among people with chronic Hepatitis B infection in Burkina Faso. Methods: rs1695 polymorphisms of GSTP1 gene genotyping was performed for 50 people infected with chronic Hepatitis B virus and 124 healthy people with the PCR-RFLP method. Conventional PCR was used for DNA amplification and Alw26I enzyme was used for enzymatic digestion. Results: The results show that the frequencies of AA, AG and GG genotypes are respectively 31.00%, 36.80% and 32.20% in general the study population with a mutation rate of 50.57%. However, the incidence of the AA, AG and GG genotypes are respectively 30.64%, 38.71% and 30.64% among people with chronic Hepatitis B virus infection and 32.00%, 32.00% and 36.00% among healthy people. In cases, the frequencies of the A and G alleles are 48.00% and 52.00% respectively, and in controls 50.00% each. No statistical difference was found by comparing genotypic and allelic frequencies between cases and controls (p > 0.05). Conclusion: Our study allowed us to determine the rate of GSTP1 rs1695 genotypes in the study population, cases and controls. From our analyses, GSTP1 rs1695 is not associated to chronic Hepatitis B virus infection in Ouagadougou.

Keywords

Polymorphism, GSTP1, Chronic Hepatitis B, Healthy People, Burkina Faso

Table 1. Sequences of primers specific to the amplification of the GSTP1 gene.

Table 2. Demographic distribution by gender and treatment.

Table 3. Demographic distribution by age group.

Table 4. Genotype frequencies of GSTP1 by demographic traits.

Table 5. Genotypic and allelic frequency of GSTP1 in cases and controls.

1. 1. Wagner, A., Denis, F., Ranger-Rogez, S., Loustaud-Ratti, V. and Alain, S. (2004) Génotypes du virus de l’hépatite B. Immuno-analyse & Biologie Spécialisée, 19, 330-342. https://doi.org/10.1016/j.immbio.2004.10.002


2. 2. Zongo, S.V., Djigma, F.W., Yonli, A.T., Sorgho, P.A., Nagalo, B.M., Traore, L., Somda, D., Amegnona, L.J., Languie, E., Some, C.C.B., Sia, L.M.J., Sourabie, I.B., Sombie, R.A., Serme, A.K., Obiri-Yeboah, D. and Simpore, J. (2023) Association of DRB1*11 and DRB1*12 Alleles of the HLA System with the Evolution of the Hepatitis B Virus Infection in Burkina Faso. Molecular Biology Reports, 50, 5039-5047. https://doi.org/10.1007/s11033-023-08353-0


3. 3. Hutin, Y., Desai, S. and Bulterys, M. (2018) Preventing Hepatitis B Virus Infection: Milestones and Targets. Bull World Health Organ, 96, 443-443A.https://doi.org/10.2471/BLT.18.215210


4. 4. OMS (2020) Hépatite B. https://www.who.int/fr/news-room/fact-sheets/detail/hepatitis-b


5. 5. Kuwahara, R., et al. (2004) Genetic Heterogeneity of the Precore and the Core Promoter Region of Genotype C Hepatitis B Virus during Lamivudine Therapy. Journal of Medical Virology, 72, 26-34. https://doi.org/10.1002/jmv.10558


6. 6. Asselah, T., Lada, O., Boyer, N., Martinot, M. and Marcellin, P. (2008) Traitement de l’hépatite chronique B. Gastroentérologie Clinique et Biologique, 32, 749-768.https://doi.org/10.1016/j.gcb.2008.07.001


7. 7. Quetier, I. and Kremsdorf, D. (2014) La protéine X du virus de l’hépatite B et son role dans le développement du carcinome hépatocellulaire. Virologie, 18, 229-238.


8. 8. Sombié, R., et al. (2010) Hépatite B chronique: aspects épidémiologique, diagnostique, thérapeutique et évolutif au centre hospitalier universitaire Yalgado Ouédraogo de Ouagadougou. Journal Africain d'Hépato-Gastroentérologie, 4, 3-10.https://doi.org/10.1007/s12157-009-0137-2


9. 9. Ouédraogo, H.G., et al. (2013) Hepatitis B Vaccination Status and Associated Factors among Health Care Workers in Burkina Faso. Médecine et Santé Tropicales, 23, 72-77. https://doi.org/10.1684/mst.2013.0157


10. 10. Tao, I., et al. (2014) Seroepidemiology of Hepatitis B and C Viruses in the General Population of Burkina Faso. Hepatitis Research and Treatment, 2014, Article ID: 781843. https://doi.org/10.1155/2014/781843


11. 11. Simpore, J., et al. (2006) Toxoplasma Gondii, HCV, and HBV Seroprevalence and Co-Infection among HIV-Positive and -Negative Pregnant Women in Burkina Faso. Journal of Medical Virology, 78, 730-733.https://doi.org/10.1002/jmv.20615


12. 12. Ilboudo, D., et al. (2010) Towards the Complete Eradication of Mother-to-Child HIV/HBV Coinfection at Saint Camille Medical Centre in Burkina Faso, Africa. The Brazilian Journal of Infectious Diseases, 14, 219-224.https://doi.org/10.1590/S1413-86702010000300004


13. 13. Diarra, B., et al. (2018) World Hepatitis Day in Burkina Faso, 2017: Seroprevalence and Vaccination against Hepatitis B Virus to Achieve the 2030 Elimination Goal. Virology Journal, 15, Article No. 121. https://doi.org/10.1186/s12985-018-1032-5


14. 14. Méda, N., Tuaillon, é., Kania, D., Tiendrebéogo, A., Pisoni, A., Zida, S., Bolloré, K., Medah, I., Laureillard, D., Molès, J.-P., Nagot, N., Nébie, K.Y., Van de Perré, P. and Dujols, P. (2018) Hepatitis B and C Virus Seroprevalence, Burkina Faso: A Cross-Sectional Study. Bulletin of the World Health Organization, 96, 750-759.https://doi.org/10.2471/BLT.18.208603


15. 15. Ghobadloo, S., Yaghmaei, B., Allameh, A., Hassani, P., Noorinayer, B. and Zali, M.R. (2006) Polymorphisms of Glutathione S-Transferase M1, T1, and P1 in Patients with HBV-Related Liver Cirrhosis, Chronic Hepatitis, and Normal Carriers. Clinical Biochemistry, 39, 46-49. https://doi.org/10.1016/j.clinbiochem.2005.10.004


16. 16. El-Serag, H.B. (2011) Hepatocellular Carcinoma. The New England Journal of Medicine, 365, 1118-1127. https://doi.org/10.1056/NEJMra1001683


17. 17. Djigma, F.W., et al. (2020) Role of Glutathione S-Transferase (GSTM1 and GSTT1) Genes Deletion in Susceptibility to HIV-1 Disease Progression. Journal of Biosciences and Medicines, 8, 41-54. https://doi.org/10.4236/jbm.2020.82004


18. 18. Ouedraogo, T., Djigma, F., Zohoncon, T., Idani, B., Ouattara, A., Sorgho, P., Obiri-Yeboah, D., Bado, P., Traore, M., Diarra, B., Yonli, A., Ouedraogo, C. and Simpore, J. (2020) Association between Polymorphisms of Glutathione S-Transferase and Progression to Cervical Cancer in Women from Burkina Faso and Mali. Journal of Biosciences and Medicines, 8, 12-25. https://doi.org/10.4236/jbm.2020.84002


19. 19. Baronica, K., et al. (2014) Progression of Multiple Sclerosis Is Associated with Gender Differences in Glutathione S-Transferase P1 Detoxification Pathway. Acta Neurobiologiae Experimentalis, 74, 257-265.


20. 20. Eum, K.-D., et al. (2015) Modification of the Association between Lead Exposure and Amyotrophic Lateral Sclerosis by Iron and Oxidative Stress Related Gene Polymorphisms. Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration, 16, 72-79. https://doi.org/10.3109/21678421.2014.964259


21. 21. Pemble, S., et al. (1994) Human Glutathione S-Transferase Theta (GSTT1): cDNA Cloning and the Characterization of a Genetic Polymorphism. Biochemical Journal, 300, 271-276. https://doi.org/10.1042/bj3000271


22. 22. Meyer, U.A. and Zanger, U.M. (1997) Molecular Mechanisms of Genetic Polymorphisms of Drug Metabolism. Annual Review of Pharmacology and Toxicology, 37, 269-296. https://doi.org/10.1146/annurev.pharmtox.37.1.269


23. 23. Kiran, B., 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


24. 24. Harries, L.W., Stubbins, M.J., et al. (1997) Identification of Genetic Polymorphisms at the Glutathione S-Transferase Pi Locus and Association with Susceptibility to Bladder, Testicular and Prostate Cancer. Carcinogenesis, 18, 641-644. https://pubmed.ncbi.nlm.nih.gov/9111193/


25. 25. Phuthong, S., Settheetham-Ishida, W., Natphopsuk, S. and Ishida, T. (2018) Genetic Polymorphism of the Glutathione S-Transferase Pi 1 (GSTP1) and Susceptibility to Cervical Cancer in Human Papilloma Virus Infected Northeastern Thai Women. Asian Pacific Journal of Cancer Prevention, 19, 381-385.


26. 26. Settheetham-Ishida, W., et al. (2004) Contribution of Epigenetic Risk Factors but Not p53 Codon 72 Polymorphism to the Development of Cervical Cancer in Northeastern Thailand. Cancer Letters, 16, 205-211. https://pubmed.ncbi.nlm.nih.gov/15183536/


27. 27. Zhao, E., Hu, K. and Zhao, Y. (2017) Associations of the Glutathione S-Transferase P1 Ile105Val Genetic Polymorphism with Gynecological Cancer Susceptibility: A Meta-Analysis. Oncotarget, 8, 41734-41739.https://doi.org/10.18632/oncotarget.16764


28. 28. Miller, S.A., Dykes, D.D. and Polesky, H.F. (1988) A Simple Salting out Procedure for Extracting DNA from Human Nucleated Cells. Nucleic Acids Research, 16, 1215. https://pubmed.ncbi.nlm.nih.gov/3344216/


29. 29. Abbas, A., et al. (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 Journal of Gastroenterology, 10, 3389-3393. https://doi.org/10.3748/wjg.v10.i23.3389


30. 30. Sombié, R., Sangaré, L., Guingané, A., Tiendrébéogo, A., Kaboré, D. and Bougouma, A. (2015) Traitement de l’hépatite B chronique par les analogues de nucléos (t) ides. Journal Africain d'Hépato-Gastroentérologie, 9, 114-118.https://doi.org/10.1007/s12157-015-0601-4


31. 31. Sawadogo, A., Kyelem, C.G., Yaméogo, T.M., Barro, L., Kamboulé, B.E. and Dahourou, H. (2015) Statut du portage du virus de l’hépatite B (VHB) au sein du personnel de santé du CHU Souro Sanou de Bobo-Dioulasso, Burkina Faso. Journal Africain d'Hépato-Gastroentérologie, 9, 30-34.https://doi.org/10.1007/s12157-014-0582-4


32. 32. Marcellin, P., Asselah, T. and Boyer, N. (2005) Treatment of Chronic Hepatitis B. Journal of Viral Hepatitis, 12, 333-345. https://doi.org/10.1111/j.1365-2893.2005.00599.x


33. 33. Kassongue, Y., Diakite, B., et al. (2022) Genetic Polymorphism of Drug Metabolism Enzymes (GSTM1, GSTT1 and GSTP1) in the Healthy Malian Population. Molecular Biology Reports, 47, 393-400. https://doi.org/10.1007/s11033-019-05143-5


34. 34. Valeeva, E.T., Mukhammadiyeva, G.F. and Bakirov, A.B. (2020) Polymorphism of Glutathione S-Transferase Genes and the Risk of Toxic Liver Damage in Petrochemical Workers. International Journal of Occupational Medicine and Environmental Health, 11, 53-58.


35. 35. de Sousa Barros, J.B., et al. (2021) No Association of GSTP1 rs1695 Polymorphism with Amyotrophic Lateral Sclerosis: A Case-Control Study in the Brazilian Population. PLOS ONE, 16, e0247024. https://doi.org/10.1371/journal.pone.0247024


36. 36. Sharma, A., et al. (2014) Genetic Polymorphism of Glutathione S-Transferase P1 (GSTP1) in Delhi Population and Comparison with Other Global Populations. Meta Gene, 2, 134-142. https://doi.org/10.1016/j.mgene.2013.12.003


37. 37. Hayes, J.D. and Pulford, D.J. (1995) The Glutathione S-Transferase Supergene Family: Regulation of GST and the Contribution of the Isoenzymes to Cancer Chemoprotection and Drug Resistance. Critical Reviews in Biochemistry and Molecular Biology, 30, 445-600. https://doi.org/10.3109/10409239509083492


38. 38. Tian, S., 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


39. 39. Palma, S., 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


40. 40. Kandemir, O., Tamer, L. and Tasdelen, B. (2008) Effects of GSTT1, GSTM1 and GSTP1 Gene Polymorphism on the Course of Hepatitis B Virus Infection. Hepatogastroenterology, 55, 1729-1733.

Conflicts of Interest

The authors declare no conflicts of interest regarding the publication of this paper.

References

[1]	Wagner, A., Denis, F., Ranger-Rogez, S., Loustaud-Ratti, V. and Alain, S. (2004) Génotypes du virus de l’hépatite B. Immuno-analyse & Biologie Spécialisée, 19, 330-342. https://doi.org/10.1016/j.immbio.2004.10.002
[2]	Zongo, S.V., Djigma, F.W., Yonli, A.T., Sorgho, P.A., Nagalo, B.M., Traore, L., Somda, D., Amegnona, L.J., Languie, E., Some, C.C.B., Sia, L.M.J., Sourabie, I.B., Sombie, R.A., Serme, A.K., Obiri-Yeboah, D. and Simpore, J. (2023) Association of DRB1*11 and DRB1*12 Alleles of the HLA System with the Evolution of the Hepatitis B Virus Infection in Burkina Faso. Molecular Biology Reports, 50, 5039-5047. https://doi.org/10.1007/s11033-023-08353-0
[3]	Hutin, Y., Desai, S. and Bulterys, M. (2018) Preventing Hepatitis B Virus Infection: Milestones and Targets. Bull World Health Organ, 96, 443-443A. https://doi.org/10.2471/BLT.18.215210
[4]	OMS (2020) Hépatite B. https://www.who.int/fr/news-room/fact-sheets/detail/hepatitis-b
[5]	Kuwahara, R., et al. (2004) Genetic Heterogeneity of the Precore and the Core Promoter Region of Genotype C Hepatitis B Virus during Lamivudine Therapy. Journal of Medical Virology, 72, 26-34. https://doi.org/10.1002/jmv.10558
[6]	Asselah, T., Lada, O., Boyer, N., Martinot, M. and Marcellin, P. (2008) Traitement de l’hépatite chronique B. Gastroentérologie Clinique et Biologique, 32, 749-768. https://doi.org/10.1016/j.gcb.2008.07.001
[7]	Quetier, I. and Kremsdorf, D. (2014) La protéine X du virus de l’hépatite B et son role dans le développement du carcinome hépatocellulaire. Virologie, 18, 229-238.
[8]	Sombié, R., et al. (2010) Hépatite B chronique: aspects épidémiologique, diagnostique, thérapeutique et évolutif au centre hospitalier universitaire Yalgado Ouédraogo de Ouagadougou. Journal Africain d'Hépato-Gastroentérologie, 4, 3-10. https://doi.org/10.1007/s12157-009-0137-2
[9]	Ouédraogo, H.G., et al. (2013) Hepatitis B Vaccination Status and Associated Factors among Health Care Workers in Burkina Faso. Médecine et Santé Tropicales, 23, 72-77. https://doi.org/10.1684/mst.2013.0157
[10]	Tao, I., et al. (2014) Seroepidemiology of Hepatitis B and C Viruses in the General Population of Burkina Faso. Hepatitis Research and Treatment, 2014, Article ID: 781843. https://doi.org/10.1155/2014/781843
[11]	Simpore, J., et al. (2006) Toxoplasma Gondii, HCV, and HBV Seroprevalence and Co-Infection among HIV-Positive and -Negative Pregnant Women in Burkina Faso. Journal of Medical Virology, 78, 730-733. https://doi.org/10.1002/jmv.20615
[12]	Ilboudo, D., et al. (2010) Towards the Complete Eradication of Mother-to-Child HIV/HBV Coinfection at Saint Camille Medical Centre in Burkina Faso, Africa. The Brazilian Journal of Infectious Diseases, 14, 219-224. https://doi.org/10.1590/S1413-86702010000300004
[13]	Diarra, B., et al. (2018) World Hepatitis Day in Burkina Faso, 2017: Seroprevalence and Vaccination against Hepatitis B Virus to Achieve the 2030 Elimination Goal. Virology Journal, 15, Article No. 121. https://doi.org/10.1186/s12985-018-1032-5
[14]	Méda, N., Tuaillon, é., Kania, D., Tiendrebéogo, A., Pisoni, A., Zida, S., Bolloré, K., Medah, I., Laureillard, D., Molès, J.-P., Nagot, N., Nébie, K.Y., Van de Perré, P. and Dujols, P. (2018) Hepatitis B and C Virus Seroprevalence, Burkina Faso: A Cross-Sectional Study. Bulletin of the World Health Organization, 96, 750-759. https://doi.org/10.2471/BLT.18.208603
[15]	Ghobadloo, S., Yaghmaei, B., Allameh, A., Hassani, P., Noorinayer, B. and Zali, M.R. (2006) Polymorphisms of Glutathione S-Transferase M1, T1, and P1 in Patients with HBV-Related Liver Cirrhosis, Chronic Hepatitis, and Normal Carriers. Clinical Biochemistry, 39, 46-49. https://doi.org/10.1016/j.clinbiochem.2005.10.004
[16]	El-Serag, H.B. (2011) Hepatocellular Carcinoma. The New England Journal of Medicine, 365, 1118-1127. https://doi.org/10.1056/NEJMra1001683
[17]	Djigma, F.W., et al. (2020) Role of Glutathione S-Transferase (GSTM1 and GSTT1) Genes Deletion in Susceptibility to HIV-1 Disease Progression. Journal of Biosciences and Medicines, 8, 41-54. https://doi.org/10.4236/jbm.2020.82004
[18]	Ouedraogo, T., Djigma, F., Zohoncon, T., Idani, B., Ouattara, A., Sorgho, P., Obiri-Yeboah, D., Bado, P., Traore, M., Diarra, B., Yonli, A., Ouedraogo, C. and Simpore, J. (2020) Association between Polymorphisms of Glutathione S-Transferase and Progression to Cervical Cancer in Women from Burkina Faso and Mali. Journal of Biosciences and Medicines, 8, 12-25. https://doi.org/10.4236/jbm.2020.84002
[19]	Baronica, K., et al. (2014) Progression of Multiple Sclerosis Is Associated with Gender Differences in Glutathione S-Transferase P1 Detoxification Pathway. Acta Neurobiologiae Experimentalis, 74, 257-265.
[20]	Eum, K.-D., et al. (2015) Modification of the Association between Lead Exposure and Amyotrophic Lateral Sclerosis by Iron and Oxidative Stress Related Gene Polymorphisms. Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration, 16, 72-79. https://doi.org/10.3109/21678421.2014.964259
[21]	Pemble, S., et al. (1994) Human Glutathione S-Transferase Theta (GSTT1): cDNA Cloning and the Characterization of a Genetic Polymorphism. Biochemical Journal, 300, 271-276. https://doi.org/10.1042/bj3000271
[22]	Meyer, U.A. and Zanger, U.M. (1997) Molecular Mechanisms of Genetic Polymorphisms of Drug Metabolism. Annual Review of Pharmacology and Toxicology, 37, 269-296. https://doi.org/10.1146/annurev.pharmtox.37.1.269
[23]	Kiran, B., 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
[24]	Harries, L.W., Stubbins, M.J., et al. (1997) Identification of Genetic Polymorphisms at the Glutathione S-Transferase Pi Locus and Association with Susceptibility to Bladder, Testicular and Prostate Cancer. Carcinogenesis, 18, 641-644. https://pubmed.ncbi.nlm.nih.gov/9111193/
[25]	Phuthong, S., Settheetham-Ishida, W., Natphopsuk, S. and Ishida, T. (2018) Genetic Polymorphism of the Glutathione S-Transferase Pi 1 (GSTP1) and Susceptibility to Cervical Cancer in Human Papilloma Virus Infected Northeastern Thai Women. Asian Pacific Journal of Cancer Prevention, 19, 381-385.
[26]	Settheetham-Ishida, W., et al. (2004) Contribution of Epigenetic Risk Factors but Not p53 Codon 72 Polymorphism to the Development of Cervical Cancer in Northeastern Thailand. Cancer Letters, 16, 205-211. https://pubmed.ncbi.nlm.nih.gov/15183536/
[27]	Zhao, E., Hu, K. and Zhao, Y. (2017) Associations of the Glutathione S-Transferase P1 Ile105Val Genetic Polymorphism with Gynecological Cancer Susceptibility: A Meta-Analysis. Oncotarget, 8, 41734-41739. https://doi.org/10.18632/oncotarget.16764
[28]	Miller, S.A., Dykes, D.D. and Polesky, H.F. (1988) A Simple Salting out Procedure for Extracting DNA from Human Nucleated Cells. Nucleic Acids Research, 16, 1215. https://pubmed.ncbi.nlm.nih.gov/3344216/
[29]	Abbas, A., et al. (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 Journal of Gastroenterology, 10, 3389-3393. https://doi.org/10.3748/wjg.v10.i23.3389
[30]	Sombié, R., Sangaré, L., Guingané, A., Tiendrébéogo, A., Kaboré, D. and Bougouma, A. (2015) Traitement de l’hépatite B chronique par les analogues de nucléos (t) ides. Journal Africain d'Hépato-Gastroentérologie, 9, 114-118. https://doi.org/10.1007/s12157-015-0601-4
[31]	Sawadogo, A., Kyelem, C.G., Yaméogo, T.M., Barro, L., Kamboulé, B.E. and Dahourou, H. (2015) Statut du portage du virus de l’hépatite B (VHB) au sein du personnel de santé du CHU Souro Sanou de Bobo-Dioulasso, Burkina Faso. Journal Africain d'Hépato-Gastroentérologie, 9, 30-34. https://doi.org/10.1007/s12157-014-0582-4
[32]	Marcellin, P., Asselah, T. and Boyer, N. (2005) Treatment of Chronic Hepatitis B. Journal of Viral Hepatitis, 12, 333-345. https://doi.org/10.1111/j.1365-2893.2005.00599.x
[33]	Kassongue, Y., Diakite, B., et al. (2022) Genetic Polymorphism of Drug Metabolism Enzymes (GSTM1, GSTT1 and GSTP1) in the Healthy Malian Population. Molecular Biology Reports, 47, 393-400. https://doi.org/10.1007/s11033-019-05143-5
[34]	Valeeva, E.T., Mukhammadiyeva, G.F. and Bakirov, A.B. (2020) Polymorphism of Glutathione S-Transferase Genes and the Risk of Toxic Liver Damage in Petrochemical Workers. International Journal of Occupational Medicine and Environmental Health, 11, 53-58.
[35]	de Sousa Barros, J.B., et al. (2021) No Association of GSTP1 rs1695 Polymorphism with Amyotrophic Lateral Sclerosis: A Case-Control Study in the Brazilian Population. PLOS ONE, 16, e0247024. https://doi.org/10.1371/journal.pone.0247024
[36]	Sharma, A., et al. (2014) Genetic Polymorphism of Glutathione S-Transferase P1 (GSTP1) in Delhi Population and Comparison with Other Global Populations. Meta Gene, 2, 134-142. https://doi.org/10.1016/j.mgene.2013.12.003
[37]	Hayes, J.D. and Pulford, D.J. (1995) The Glutathione S-Transferase Supergene Family: Regulation of GST and the Contribution of the Isoenzymes to Cancer Chemoprotection and Drug Resistance. Critical Reviews in Biochemistry and Molecular Biology, 30, 445-600. https://doi.org/10.3109/10409239509083492
[38]	Tian, S., 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
[39]	Palma, S., 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
[40]	Kandemir, O., Tamer, L. and Tasdelen, B. (2008) Effects of GSTT1, GSTM1 and GSTP1 Gene Polymorphism on the Course of Hepatitis B Virus Infection. Hepatogastroenterology, 55, 1729-1733.