Can the SNP on TCF19 and POU5F1 predict risk in allopurinol-induced severe cutaneous adverse drug reactions in Thai Patients?

Authors

  • Thawinee Jantararoungtong
  • Gaidganok Sornsamdang
  • Santirat Prommas
  • Napatrupron Koomdee
  • Apichaya Puangpetch
  • Patompong Satapornpong
  • Therdpong Tempark
  • Pawinee Rerknimitr
  • Jettanong Klaewsongkram
  • Papapit Tuchinda
  • Leena Chularojanamontri
  • Napatra Tovanabutra
  • Kumutnart Chanprapaph
  • Wareeporn Disphanurat
  • Panlop Chakkavittumrong
  • Chutika Srisuttiyakorn
  • Ticha Rerkpattanapipat
  • Chonlaphat Sukasem Division of Pharmacogenomics and Personalized Medicine Department of Pathology, Faculty of Medicine, Mahidol University, Thailand

DOI:

https://doi.org/10.14456/gag.2020.7

Keywords:

HLA-B*58:01; allopurinol; Thai; SCAR; cADR; drug hypersensitivity

Abstract

The aim of this study was to investigate the association of Human leukocyte antigen B (HLA-B), Transcription Factor 19 (TCF19) and POU Class 5 Homeobox 1 (POU5F1) genes with allopurinol-induced cutaneous adverse drug reactions (cADRs), including Stevens-Johnson syndrome/ toxic epidermal necrosis (SJS/TEN; n=21), drug rash with eosinophilia and systemic symptoms (DRESS; n=16) and maculopapular exanthema (MPE; n=7) in Thai patients. This case-control association study compares 44 cases with allopurinol-induced cADR with allopurinol-tolerant control patients (n=100) and a population control group (n=1,095). The control group comprised patients who had received allopurinol for more than 6 months without any adverse cutaneous event. HLA alleles were genotyped using a two-stage sequence-specific oligonucleotide probe system (PCR-SSOP).Variants in TCF19 (rs9263794 and rs1044870) and POU5F1 (rs9263796) were genotyped. The risk of allopurinol-induced cADR was significantly higher in the patients with HLA-B*58:01 allele with an odds ratio 240 (95%CI: 57.19–1007.08, p<0.001). In addition, the single nucleotide polymorphisms were also significantly associated with the allopurinol-induced cADR (rs9263794; OR 57.20, p< 0.001, rs1044870; OR 77.31, p< 0.001 and rs9263796; OR 84.14, p<0.001) Furthermore, we found that gender, at the initiation of treatment was associated with allopurinol-induced cADR (OR 59.00, 95%CI: 19.57–98.42, p<0.01). These results suggest that screening tests for HLA-B*58:01 alleles in patients who will be treated with low dosage of allopurinol will be clinically helpful in preventing the risk of developing DRESS, SJS/TEN and MPE in Thai population.

Author Biography

Chonlaphat Sukasem, Division of Pharmacogenomics and Personalized Medicine Department of Pathology, Faculty of Medicine, Mahidol University, Thailand

Research Publications

  1. Sukasem C, Churdboonchart V, Chasombat S, Kohreanudom S, Watitpun C, Pasomsub E, Piroj W, Tiensuwan M, Chantratita W. Surveillance of genotypic    resistance mutations in HIV-1 treated individuals after completion of the National Access to Antiretroviral Program in Thailand. Infection 2010; 35: 81-88.
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  3. Sukasem C, Churdboonchart V, Sirisidthi K, Riengrojpitak S, Chasombat S, Watitpun C, Piroj W, Tiensuwan M, Chantratita W. Genotypic resistance mutations in treatment-naïve and treatment-experienced patients under widespread use of antiretroviral drug in Thailand: Implication for further epidemiologic surveillance. Jpn J Infect Dis. 2007; 60: 284-289.
  4. Sukasem C, Churdboonchart V, Sukeepaisarncharoen W, Piroj W, Inwisai T, Tiensuwan M, Chantratita W. Genotypic resistance profiles in antiretroviral-naive HIV-1 infections before and after initiation of first-line HAART: Impact of polymorphism on therapy resistance. Int J Antimicrob Agents. 2008; 31: 277-281.
  5. Sukasem C, Srichunrusami C, Keatkla J, Tiensuwan M, Chantratita W. The presence of anti-R7V antibodies in HIV-infected patients: a novel marker for the non-progression to AIDS”, Abstract for the 8th International Meeting on Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases. Infection, Genetics and Evolution 2008: S1–S49.
  6. Chantratita W, Sukasem C, Kaewpongsri S, Srichunrusami C, Pairoj W, Thitithanyanont A, Chaichoune K, Ratanakron P, Songserm T, Damrongwatanapokin S, Landt O. Qualitative detection of avian influenza A (H5N1) viruses: a comparative evaluation of four real time nucleic acid amplification methods. Mol Cell Probes. 2008; 22:287-294.
  7. Sungkanuparph S, Sukasem C, Manosuthi W, Wiboonchutikul S, Piyavong B, Chantratita W.  Tipranavir resistance in protease inhibitor-naïve patients with HIV-1 subtype A/E infection. J Clin Virol. 2008; 43:284-286.  
  8. Manosuthi W, Butler DM, Chantratita W, Sukasem C, Richman DD, Smith DM. Patients infected with HIV-1 subtype CRF01_AE and failing first-line Nevirapine- and Efavirenz- based regimens demonstrate consideration cross resistance to Etravirine. AIDS Res Hum Retroviruses 2010; 26: 609-611.
  9. Kiertiburanakul S, Wiboonchutikul S, Sukasem C, Chantratita W, Sungkanuparph S. Using of nevirapine is associated with intermediate and reduced response to etravirine among HIV-infected patients who experienced virologic failure in a resource-limited setting. J Clin Virol. 2010; 47: 330-334.
  10. Pasomsub E, Sukasem C, Sungkanuparph S, Kijsirikul B, Chantratita W.The Application of Artificial Neural Networks for Phenotypic Drug Resistance Prediction: Comparison and Evaluation with the Interpretation Systems Based on Genotype Resistance Mutations. Jpn J Infect Dis. 2010; 63: 87-94. 
  11. Wiboonchutikul S, Sungkanuparph S, Sukasem C, Wathipthun C, Chantratita W. Comparison of  Protease Inhibitor (PI) Resistance-associated Mutations between PI-naïve and PI-experienced HIV-1 Infected Patients in Thailand Where Subtype A/E is Predominant. Curr HIV Res. 2010; 8: 456-60.
  12. Panichakul T, Thophon S, Kakhai C, Sukasem C. Surveillance and prevention of enterovirus spreading and hand-foot-mouth disease occurrence in young children. Journal of Public Health and Development 2010; 8: 2.
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  16. Sukasem C. Pharmacogenetic Markers to Predict Drug-induced Allergic Reactions. Review article, Thai Pharmaceutical and Health Science Journal,2010; 4: 532-538.
  17. Chantratita W, Sukasem C, Sirinavin S, Sankuntaw N, Srichantaratsamee C, Pasomsub E, Malathum K. Simultaneous detection and subtyping of H274Y-positive influenza A (H1N1) using pyrosequencing. J Infect Dev Ctries. 2011; 28;5(5):348-52.
  18. Pongthanapisith V, Sukasem C, Premchaiporn K, Srichantaratsamee C, Chantratita W. Evaluation of three rapid diagnostic tests for influenza virus in nasopharyngeal specimens during an outbreak of novel swine-origin influenza viruses in Thailand. Infection. 2011;39(2):105-11. (Co-first authorship)
  19. Srisawasdi P, Chaloeysup S, Teerajetgul Y, Pocathikorn A, Sukasem C, Vanavanan S, Kroll MH. Estimation of plasma small dense LDL cholesterol from classic lipid measures. Am J Clin Pathol. 2011;136(1):20-9.
  20. Sungkanuparph S, Kiertiburanakul S, Sukasem C, Chantratita W. Discrepancies between WHO 2009 and IAS-USA 2009 lists for determining the rate of transmitted HIV-1 drug resistance: A prospective study. J Acquir Immune Defic Syndr. 2012; 59(1):e3-5.
  21. Sungkanuparph S, Sukasem C, Kiertiburanakul S, Pasomsub E, Chantratita W. Emergence of HIV-1 drug resistance mutations among antiretroviral-naive HIV-1-infected patients after rapid scaling up of antiretroviral therapy in Thailand. J Int AIDS Soc. 2012; 12:12.
  22. Sukasem C, Prapaithong P., Pasomsub E., Srichunrusami C., Cressey TR., Jantararoungtong T., Chantratita W. Pharmacogenetic markers of CYP2B6 associated with efavirenz plasma concentrations in HIV-1 infected Thai adults.Br J Clin Pharmacol. 2012 Dec;74(6):1005-12.
  23. Punyacam P, Iemwimangsa N, Chantratita W, Sukasem C, Sungkanuparph S. HIV Drug Resistance Interpreted by Cumulative Versus Last Genotypes in HIV-Infected Patients with Multiple Treatment Failures. Curr HIV Res. 2012 Apr 1;10(3):271-4.
  24. Sirachainan E, Jaruhathai S, Trachu N, Panvichian R, Sirisinha T, Ativitavas T, Ratanatharathorn V, Sukasem C. CYP2D6 polymorphisms influences the efficacy of adjuvant Tamoxifen in Thai breast cancer patients. Pharmgenomics Pers Med. 2012;5:149-53.
  25. Sukasem C. Sirachainan E, Pechatanan K, Chamnanphon M., Sirisinha T, Ativitavas T, Panvichian R, Ratanatharathorn V, Sansorn I., Chantratita W, Impact of CYP2D6 polymorphisms on tamoxifen response of woman with breast cancer: A microarray-based study in Thailand. Asian Pac J Cancer Prev. 2012;13(9):4549-53.
  26. Sirachainan E, Reungwetwattana T, Trachu N, Wisetpanit Y, Panvichian R, Sirisinha T, Ativitavas T, Ratanatharathorn V, Sukasem C. Pharmacogenetic study of 5-Fluorouracil-related severe toxicity in Thai cancer patients: a novel SNP detection. J Pharmacogenom Pharmacoproteomics. 2012; 3:112.
  27. Tan-kam T, Suthisisang C, Pawasuthipaisit C, Limsila P, Sukasem C. Use of Pharmacogenetics in the Treatment of Children with Attention Deficit Hyperactive Disorder in Thailand Pharmgenomics Pers Med. 2013;6:3-7.
  28. Manosuthi W, Sukasem C, Lueangniyomkul A, Mankatitham W, Thongyen S, Nilkamhang S, Manosuthi S, Sungkanuparph S. Impact of Pharmacogenetic Markers of CYP2B6, Clinical Factors, and Drug-Drug Interaction on Efavirenz Levels in HIV/Tuberculosis Co-Infected Patients. Antimicrob Agents Chemother. 2013; 57:1019-24.
  29. Sukasem C, Chamnanphol M, Koomdee N, Puangpetch A, Santon S, Jantararoungtong T, Prommas S, Manosuthi W. High Plasma Efavirenz Concentration and CYP2B6 Polymorphisms in Thai HIV-1 Infections. Drug Metab Pharmacokinet. 2013 Feb 12. [Epub ahead of print].
  30. Tunthong R, Vathesatogkit P, Sukasem C, Puangpetch A, Chantratita W, Angchaisuksiri P, Sura T, Pathumarak A, Yamwong S, Boonbaichaiyapruck S, Sritara P. Pharmacogenetic study of CYP 2C19 and clopidogrel dose adjustment according to platelet reactivity monitoring in atherothrombotic-risk patients in Thailand. Curr Pharmacogenomics Person Med. 2013; 11: 154-161.
  31. Chamnanphon M, Sensorn I, Sirachainan E, Trachu N, Chantratita W, Pasomsub E, Noonpakdee W, Sukasem C. Association of CYP2D6 and CYP2C19 polymorphisms and disease-free survival of Thai post-menopausal breast cancer patients who received adjuvant tamoxifen. Pharmgenomics Pers Med. 2013 May 24; 6:37-48.
  32. Srisawasdi P, Suwalak T, Sukasem C, Chittamma A, Pocathikorn A, Vanavanan S, Puangpetch A, Santon S, Chantratita W, Kiertiburanakul S, Kroll MH. Small-Dense LDL Cholesterol/Large-Buoyant LDL Cholesterol Ratio as an Excellent Marker for Indicating Lipodystrophy in HIV-Infected Patient. Am J Clin Pathol. 2013 Oct;140 (4):506-15.
  33. Sukasem C, Gatrungsei M, Promso S, Cunningham P, Koomdee N, Chamnanphon M, Chantratita W. Evaluation of a Pharmacogenetic Test in Thailand for Abacavir Hypersensitivity Screening in Human immunodeficiency Virus Infection. Curr Pharmacogenomics Person Med. 2013, 11(4): 231-236.
  34. Sensorn I, Jantararoungtong T, Sirachainan E, Chamnanphol M, Trachu N, Pasomsub E, Supavilai P, Pinthong D, Sukasem C. Association of CYP3A, ABCB1 and ABCC2 Polymorphisms and Clinical outcomes of Thai Breast cancer Patients treated with Tamoxifen. Pharmgenomics Pers Med. 2013 Aug 26;6:93-8.
  35. Sukasem C, Tunthong R, Poungpetch A, Pairoj V, Srichunrasami C, Santon S, Vathesatogkit P, Chantratita W. CYP2C19 polymorphisms in Thai population and their clinical response to clopidogrel in patients with atherothrombotic-risk factors. Pharmgenomics Pers Med. 2013:6 85–91.
  36. Sukasem C and Sungkanuparph S. Would a CYP2B6 test help HIV patients being treated with Efavirenz?, Pharmacogenomics. 2013 Jul;14(9):999-1001.
  37. Suwannarat P, Chamnanphon M, Ngamsamut N, Sinrachatanant A, Chamkrachchangpada B, Tan-kam T, Puangpetch A, Sukasem C, Limsila P. Molecular genetic analysis of CYP2D6 and HLA-B*15:02 in Thai autistic spectrum disorder children: Implication for pharmacogenetics testing and optimization of drug treatments. Thai J. Genet. 2013, 6(1): 81-85.
  38. Wongkittichote P, Sukasem C, Kikuchi A, Aekplakorn W, Jensen LT, Kure S, Wattanasirichaigoon D. Screening of SLC25A13 Mutations in The Thai Population. World J Gastroenterol. 2013 Nov 21;19(43):7735-42.
  39. Puangpetch A, Sukasem C, Chamnanpol M, Jantararoungtong T, Koomdee N, Santon S and Prommas S (2013). HLA-B allele frequencies in Thai population. Front. Immunol. 2013.
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  41. Manosuthi W, Sukasem C, Mankatitham W, Lueangniyomkul A, Thongyen S, Nilkamhang S, Manosuthi S, Sungkanuparph S. CYP2B6 18492T>C Polymorphism Compromises Efavirenz-based Antiretroviral Regimen in Co-infected HIV and Tuberculosis Patients Carrying CYP2B6 Haplotype *1/*1. Antimicrob Agents Chemother. 2014 Apr;58(4):2268-73. 
  42. Sukasem C, Manosuthi W, Koomdee N, Santon S, Jantararoungtong T, Prommas S, Chamnanphol M, Puangpetch A. Sungkanuparph S. Low level of efavirenz in HIV-1 infected Thai adults are associated with CYP2B6 polymorphism. Infection. 2014. June; 42 (3) (2014), 469-74
  43. Sukasem C, Chamnanphol M, Koomdee N, Santon S, Jantararoungtong T, Prommas S, , Puangpetch A. Manosuthi W. Sungkanuparph S. Pharmacogenetics and clinical biomarkers for subtherapeutic plasma efavirenz concentration in HIV-1 infected Thai adults. Drug Metab Pharmacokinet. 2014 Aug 25;29(4):289-95.
  44. Manosuthi W, Sukasem C, Thongyen S, Nilkamhang S, Sungkanuparph S. ABCC2*1C and plasma tenofovir concentration are correlated to decreased glomerular filtration rate in patients receiving a tenofovir-containing antiretroviral regimen. J Antimicrob Chemother. 2014 Aug;69(8):2195-201.
  45. Suwalak T, Srisawasdi1 P, Puangpetch A, Santon S, Koomdee N, Jantararoungtong T, Prommas S, Chamnanphon M, Chantratita W, Sukasem C. The distribution of apolipoprotein E gene polymorphism and their influences in dyslipidemias in HIV-1 infections. Jpn J Infect Dis. 2014 (Accepted: In press).
  46. Sukasem C,Puangpetch A, Medhasi S, Tassaneeyakul W. Pharmacogenomics of drug-induced hypersensitivity reactions: Challenges, Opportunities and Clinical Implementation. Asian Pac J Allergy Immunol. 2014 Jun;32(2):111-23.
  47. Sukasem C, Rerkpattanapipat T, Jantararoungtong T, Prommas S, Koomdee N, Santon S, et al. HLA-B*58:01 allele is strongly associated with allopurinol–induced severe cutaneous adverse reactions in a Thai population. Clinical and Translational Allergy 2014, 4 (Suppl 3).
  48. Sukasem C, Ngamsamut N, Rerkpattanapipat T, Sinrachatanant A, Chamkrachchangpada B, Tan-kam T, Chamnanphon M,  Puangpetch A, Limsila P. Association between HLA-B*1502 allele and aromatic antiepileptic drugs-induced cutaneous adverse drug reactions and the HLA-B*15:02 pharmacogenetics screening in autistic spectrum disorder. Clinical and Translational Allergy 2014, 4 (Suppl 3).
  49. Sukasem C,  Koomdee N, Rerkpattanapipat T, Jantararoungtong T, , Prommas S, Santon S, Chamnanphol M, Puangpetch A. HLA-B*15:02 genotype associated with hypersensitivity syndrome to Lamotrigine in Thai population. Clinical and Translational Allergy 2014, 4 (Suppl 3).
  50. SukasemC, Atasilp C, Chansriwong P, ChamnanphonM, PuangpetchA, SirachainanE. Development of pyrosequencing method for detection of UGT1A1 polymorphisms in Thai colorectal cancers. J Clin Lab Anal. 2014 (Accepted: In press).
  51. HongkaewY, NgamsamutN, PuangpetchA, VanwongN, SrisawasdiP, ChamnanphonM, ChamkrachchangpadaB, Tan-kamT, LimsilaP, SukasemC. Hyperprolactinemia in Thai children and adolescences with autistic spectrum disorder treated with risperidone. Neuropsychiatr Dis Treat, 2014. (Accepted: In press).
  52. Hongkaew Y, Ngamsamut N, Puangpetch A, Vanwong N, Srisawasdi P, Chamnanphon M, Chamkrachchangpada B, Tan-kam T, Limsila P, Sukasem C. Prolactin response to risperidone in Thai children and adolescences with autistic spectrum disorder. Thai Journal of Pharmacology, 2014; 36(1). (Accepted: In press).
  53. Vanwong N, Medhasi S, Pongchaidecha M, Ngamsamut N, Puangpetch A, Chamnanphon M, Chamkrachchangpada B, Tan-kam T, Hongkaew Y, Limsila P, Sukasem C. Pharmacogenetics and clinical risk factors for risperidone-related weight gain in Thai children and adolescences with autistic spectrum disorder. Thai Journal of Pharmacology, 2014; 36(1). (Accepted: In press).
  54. Puangpetch A, Jantararoungtong T, Koomdee N, Chamnanphol M, Santon S, Prommas S, Sukasem C. HLA-B allele and haplotype diversity among Thai patients identified by PCR-SSOP: evidence for high risk of drug-induced hypersensitivity. Front. Genet, 2014 (Manuscript: revised submitted).  
  55. Barusrux B, Koomdee N, Santon S, Jantararoungtong T, Prommas S, Chamnanphol M, Puangpetch A, Sukasem C. A tendency toward higher plasma efavirenz concentration in carriers of the transporter genes ABCB1 c.3435 C>T polymorphism in HIV-1 infected Thai adults. Pharmgenomics Pers Med. 2014 (Manuscript: Submitted).                                                                      
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  57. Vanwong N, Ngamsamut N, Medhasi S, Puangpetch A, Chamnanphon M, Chamkrachchangpada B, Tan-kam T, Hongkaew Y, Limsila P, Sukasem C. Effect of CYP2D6 on risperidone pharmacokinetics in Thai Children and Adolescences with Autistic Spectrum Disorder. Pharmacogenet Genomics, 2014 (Manuscript: Submitted).
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  59. Sukasem C, Chitasombat MN, Puangpetch A, Jantararoungtong T, Chamnanphon M, Koomdee N, Santon S, Prommas S, Chuwongwatana S, Watcharananan S, Effect of CYP2C19 polymorphisms on voriconazole plasma level in Thai adult patients with invasive fungal infection. Drug Metab Pharmacokinet, 2014 (Manuscript: Submitted).
  60. Medhasi S, Vanwong N, Ngamsamut N, Puangpetch A, Chamnanphon M, Chamkrachchangpada B, Tan-kam T, Hongkaew Y, Pinthong D, Limsila P, Sukasem C. Genetic variation in metabolizing enzyme and transporter genes in Thai children and adolescences with autistic spectrum disorder: implication for pharmacogenomics-based personalized medicine. J Clin Psychopharmacol., 2014 (Manuscript: Submitted).
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2020-11-30

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Vol. 13 No. 2&3 (2020): MAY - DEC 2020

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