Advertisement

Role of human leukocyte antigen in anti-epileptic drugs-induced Stevens–Johnson Syndrome/toxic epidermal necrolysis: A meta-analysis

Published:September 16, 2022DOI:https://doi.org/10.1016/j.seizure.2022.09.011

      Highlights

      • HLA polymorphism has a strong association in AED induced SJS/TEN.
      • Asian population is more prominent to HLA polymorphism when compared to others.
      • Carbamazepine and phenytoin induced SJS/TEN were high in those with various HLA alleles polymorphism.

      Abstract

      Purpose

      Antiepileptic drugs (AEDs) are extensively used to manage epilepsy and other comorbidities associated with seizures. Human Leukocyte Antigen (HLA) has a strong association with AED-induced severe cutaneous adverse drug reactions.

      Objective

      We aimed to perform a systematic review and meta-analysis to identify, critically evaluate, and synthesize the best possible evidence on HLA-associated AED-induced Stevens–Johnson Syndrome/Toxic Epidermal Necrolysis (SJS/TEN).

      Methods

      MEDLINE/PubMed, Scopus, and the Cochrane Library were searched for literature from inception up to July 2022. We included case control studies analyzing association between HLA and AED-induced SJS/TEN. We assessed the studies’ risk of bias in using Quality of genetic studies (Q-genie) tool. Outcomes focused on association (risk) between HLA and AED-induced SJS/TEN. The estimated risk was presented in the form of odds ratio (OR).

      Results

      We included 37 studies (51,422 participants; 7027 cases and 44,395 controls). There was a significantly higher risk of Carbamazepine-induced SJS/TEN with HLA-A (OR: 1.50; 95% CI: 1.03 to 2.17), HLA-B (OR: 1.94; 95% CI: 1.45 to 2.58), HLA-C (OR: 7.83; 95% CI: 4.72 to 12.98), and HLA-DRB1 (OR: 2.82; 95% CI: 1.94 to 4.12). Lamotrigine-induced SJS/TEN posed a higher risk with HLA-A (OR: 2.38; 95% CI: 1.26 to 4.46) and HLA-B (OR: 2.79; 95% CI: 1.75 to 4.46). Phenytoin-induced SJS/TEN showed a higher risk with HLA-A (OR: 3.47; 95% CI: 2.17 to 5.56), HLA-B (OR: 1.72; 95% CI: 1.38 to 2.15), and HLA-C (OR: 2.92; 95% CI: 1.77 to 4.83). Phenobarbital-induced SJS/TEN had a higher risk with HLA-A (OR: 6.98; 95% CI: 1.81 to 26.84), HLA-B (OR: 2.40; 95% CI: 1.39 to 4.17), and HLA-C (OR: 3.37; 95% CI: 1.03 to 11.01). Zonisamide-induced SJS/TEN was significantly associated with HLA-A*02:07 (OR: 9.77; 95% CI: 3.07 to 31.1), HLA-B*46:01 (OR: 6.73; 95% CI: 2.12 to 21.36), and HLA-DRB1×08:03 (OR: 3.78; 95% CI: 1.20 to 11.97). All other alleles of HLA were observed to have a non-significant association with AED-induced SJS/TEN. All included studies were of good quality, with a score of >50 and a mean score of 54.96 out of 77.

      Conclusion

      Our study showed a significant association between few variants of HLA alleles and AED-induced SJS/TEN. Evidences from our study could help in population-based studies and in implementation of individualized treatment regimens. These findings could be part of translational research helping in precision therapy.

      Keywords

      Abbreviations:

      ADR (Adverse drug reaction), AED (Anti-epileptic drugs), CBZ (Carbamazepine), CI (Confidence interval), DRESS (Drug reaction with eosinophilia and systemic symptoms), GBP (Gabapentin), HLA (Human leukocyte antigen), LTG (Lamotrigine), LVT (Levetiracetam), MHC (Major histocompatibility complex), MPE (Maculopapular exanthema), OR (Odds ratio), PB (Phenobarbital), PHT (Phenytoin), SCARD (Severe cutaneous adverse drug reaction), SJS (Stevens-Johnson Syndrome), TEN (Toxic epidermal necrolysis), VPA (Valproic acid), ZNS (Zonisamide)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Seizure - European Journal of Epilepsy
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Sander J.W.
        The use of antiepileptic drugs—principles and practice.
        Epilepsia. 2004; 45 (Suppl): 28-34https://doi.org/10.1111/j.0013-9580.2004.455005.x
        • Rashid M.
        • Kashyap A.
        • Undela K.
        Valproic acid and Stevens–Johnson syndrome: a systematic review of descriptive studies.
        Int J Dermatol. 2019; 58: 1014-1022https://doi.org/10.1111/ijd.14411
        • Rashid M.
        • Rajan A.K.
        • Chhabra M.
        • Kashyap A.
        Levetiracetam and cutaneous adverse reactions: a systematic review of descriptive studies.
        Seizure. 2020; 75: 101-109https://doi.org/10.1016/j.seizure.2020.01.002
        • Krall R.L.
        • Penry J.K.
        • Kupferberg H.J.
        • Swinyard E.A.
        Antiepileptic drug development: I. History and a program for progress.
        Epilepsia. 1978; 19: 393-408https://doi.org/10.1111/j.1528-1157.1978.tb04506.x
        • Löscher W.
        • Schmidt D.
        Modern antiepileptic drug development has failed to deliver: ways out of the current dilemma.
        Epilepsia. 2011; 52: 657-678https://doi.org/10.1111/j.1528-1167.2011.03024.x
        • Chung W.H.
        • Wang C.W.
        • Dao R.L.
        Severe cutaneous adverse drug reactions.
        J Dermatol. 2016; 43: 758-766https://doi.org/10.1111/1346-8138.13430
        • Carey B.S.
        • Poulton K.V.
        • Poles A.
        Factors affecting HLA expression: a review.
        Int J Immunogenet. 2019; 46: 307-320https://doi.org/10.1111/iji.12443
        • Chang C.-.J.
        • Chen C.-.B.
        • Hung S.-.I.
        • Ji C.
        • Chung W.-.H
        Pharmacogenetic testing for prevention of severe cutaneous adverse drug reactions.
        Front Pharmacol. 2020; 11: 969https://doi.org/10.3389/fphar.2020.00969
        • Lin C.W.
        • Huang W.I.
        • Chao P.H.
        • Chen W.W.
        • Hsiao F.Y.
        Temporal trends and patterns in carbamazepine use, related severe cutaneous adverse reactions, and HLA-B*15:02 screening: a nationwide study.
        Epilepsia. 2018; 59: 2325-2339https://doi.org/10.1111/epi.14599
        • Grover S.
        • Kukreti R.
        HLA alleles and hypersensitivity to carbamazepine: an updated systematic review with meta-analysis.
        Pharmacogenet Genom. 2014; 24: 94-112https://doi.org/10.1097/FPC.0000000000000021
        • Ramírez E.
        • Bellón T.
        • Tong H.Y.
        • Borobia A.M.
        • de Abajo F.J.
        • Lerma V.
        • et al.
        Significant HLA class I type associations with aromatic antiepileptic drug (AED)-induced SJS/TEN are different from those found for the same AED-induced DRESS in the Spanish population.
        Pharmacol Res. 2017; 115: 168-178https://doi.org/10.1016/j.phrs.2016.11.027
        • Park H.W.
        • Kim S.H.
        • Chang Y.S.
        • Kim S.H.
        • Jee Y.K.
        • Lee A.Y.
        • et al.
        The Fas signaling pathway is a common genetic risk factor for severe cutaneous drug adverse reactions across diverse drugs.
        Allergy Asthma Immunol Res. 2018; 10: 555-561https://doi.org/10.4168/aair.2018.10.5.555
        • Chung W.H.
        • Hung S.I.
        • Hong H.S.
        • Hsih M.S.
        • Yang L.C.
        • Ho H.C.
        • et al.
        Medical genetics: a marker for Stevens–Johnson syndrome.
        Nature. 2004; 428: 486https://doi.org/10.1038/428486a
        • McCormack M.
        • Alfirevic A.
        • Bourgeois S.
        • Farrell J.J.
        • Kasperavičiūtė D.
        • Carrington M.
        • et al.
        HLA-A*3101 and carbamazepine-induced hypersensitivity reactions in Europeans.
        N Engl J Med. 2011; 364: 1134-1143https://doi.org/10.1056/NEJMoa1013297
        • Hsiao Y.H.
        • Hui R.C.
        • Wu T.
        • Chang W.C.
        • Hsih M.S.
        • Yang C.H.
        • et al.
        Genotype-phenotype association between HLA and carbamazepine-induced hypersensitivity reactions: strength and clinical correlations.
        J Dermatol Sci. 2014; 73: 101-109https://doi.org/10.1016/j.jdermsci.2013.10.003
        • Chen C.B.
        • Hsiao Y.H.
        • Wu T.
        • Hsih M.S.
        • Tassaneeyakul W.
        • Jorns T.P.
        • et al.
        Risk and association of HLA with oxcarbazepine-induced cutaneous adverse reactions in Asians.
        Neurology. 2017; 88: 78-86https://doi.org/10.1212/WNL.0000000000003453
        • Sukasem C.
        • Chaichan C.
        • Nakkrut T.
        • Satapornpong P.
        • Jaruthamsophon K.
        • Jantararoungtong T.
        • et al.
        Association between HLA-B alleles and carbamazepine-induced maculopapular exanthema and severe cutaneous reactions in Thai patients.
        J Immunol Res. 2018; 20182780272https://doi.org/10.1155/2018/2780272
        • An D.M.
        • Wu X.T.
        • Hu F.Y.
        • Yan B.
        • Stefan H.
        • Zhou D.
        Association study of lamotrigine-induced cutaneous adverse reactions and HLA-B*1502 in a Han Chinese population.
        Epilepsy Res. 2010; 92: 226-230https://doi.org/10.1016/j.eplepsyres.2010.10.006
        • Li L.J.
        • Hu F.Y.
        • Wu X.T.
        • An D.M.
        • Yan B.
        • Zhou D
        Predictive markers for carbamazepine and lamotrigine-induced maculopapular exanthema in Han Chinese.
        Epilepsy Res. 2013; 106: 296-300https://doi.org/10.1016/j.eplepsyres.2013.05.004
        • Koomdee N.
        • Pratoomwun J.
        • Jantararoungtong T.
        • Theeramoke V.
        • Tassaneeyakul W.
        • Klaewsongkram J.
        • et al.
        Association of HLA-A and HLA-B alleles with lamotrigine-induced cutaneous adverse drug reactions in the Thai population.
        Front Pharmacol. 2017; 8: 879https://doi.org/10.3389/fphar.2017.00879
        • Ihtisham K.
        • Ramanujam B.
        • Srivastava S.
        • Mehra N.K.
        • Kaur G.
        • Khanna N.
        • et al.
        Association of cutaneous adverse drug reactions due to antiepileptic drugs with HLA alleles in a North Indian population.
        Seizure. 2019; 66: 99-103https://doi.org/10.1016/j.seizure.2019.02.011
        • Ramanujam B.
        • Ihtisham K.
        • Kaur G.
        • Srivastava S.
        • Mehra N.K.
        • Khanna N.
        • et al.
        Spectrum of cutaneous adverse reactions to Levetiracetam and human leukocyte antigen typing in North-Indian patients.
        J Epilepsy Res. 2016; 6: 87-92https://doi.org/10.14581/jer.16016
        • Li W.
        • Wang J.
        • Lin H.
        • Shen G.
        HLA-A∗24:02 associated with lamotrigine-induced cutaneous adverse drug reactions: a systematic review and meta-analysis.
        Medicine (Baltimore). 2020; 99: e23929https://doi.org/10.1097/MD.0000000000023929
        • Nicoletti P.
        • Barrett S.
        • McEvoy L.
        • Daly A.K.
        • Aithal G.
        • Lucena M.I.
        • et al.
        Shared genetic risk factors across carbamazepine-induced hypersensitivity reactions.
        Clin Pharm Ther. 2019; 106: 1028-1036https://doi.org/10.1002/cpt.1493
        • Deng Y.
        • Li S.
        • Zhang L.
        • Jin H.
        • Zou X.
        Association between HLA alleles and lamotrigine-induced cutaneous adverse drug reactions in Asian populations: a meta-analysis.
        Seizure. 2018; 60: 163-171https://doi.org/10.1016/j.seizure.2018.06.024
        • Chouchi M.
        • Kaabachi W.
        • Tizaoui K.
        • Daghfous R.
        • Aidli S.E.
        • Hila L.
        The HLA-B*15:02 polymorphism and Tegretol(®)-induced serious cutaneous reactions in epilepsy: an updated systematic review and meta-analysis.
        Rev Neurol. 2018; 174: 278-291https://doi.org/10.1016/j.neurol.2017.11.006
        • Tangamornsuksan W.
        • Scholfield N.
        • Lohitnavy M.
        Association between HLA genotypes and oxcarbazepine-induced cutaneous adverse drug reactions: a systematic review and meta-analysis.
        J Pharm Pharm Sci. 2018; 21: 1-18https://doi.org/10.18433/J36S7D
        • Liu Y.
        • Yu Y.
        • Nie X.
        • Zhao L.
        • Wang X.
        Association between HLA-B*15:02 and oxcarbazepine-induced cutaneous adverse reaction: a meta-analysis.
        Pharmacogenomics. 2018; 19: 547-552https://doi.org/10.2217/pgs-2017-0189
        • Wang Q.
        • Sun S.
        • Xie M.
        • Zhao K.
        • Li X.
        • Zhao Z.
        Association between the HLA-B alleles and carbamazepine-induced SJS/TEN: a meta-analysis.
        Epilepsy Res. 2017; 135: 19-28https://doi.org/10.1016/j.eplepsyres.2017.05.015
        • Shi Y.W.
        • Min F.L.
        • Zhou D.
        • Qin B.
        • Wang J.
        • Hu F.Y.
        • et al.
        HLA-A*24:02 as a common risk factor for antiepileptic drug-induced cutaneous adverse reactions.
        Neurol. 2017; 88: 2183-2191https://doi.org/10.1212/WNL.0000000000004008
        • Li X.
        • Yu K.
        • Mei S.
        • Huo J.
        • Wang J.
        • Zhu Y.
        • et al.
        HLA-B*1502 increases the risk of phenytoin or lamotrigine induced Stevens–Johnson Syndrome/toxic epidermal necrolysis: evidence from a meta-analysis of nine case-control studies.
        Drug Res. 2015; 65: 107-111https://doi.org/10.1055/s-0034-1375684
        • Génin E.
        • Schumacher M.
        • Roujeau J.C.
        • Naldi L.
        • Liss Y.
        • Kazma R.
        • et al.
        Genome-wide association study of Stevens–Johnson syndrome and toxic epidermal necrolysis in Europe.
        Orphanet J Rare Dis. 2011; 6: 52https://doi.org/10.1186/1750-1172-6-52
        • Yip V.L.
        • Alfirevic A.
        • Pirmohamed M.
        Genetics of immune-mediated adverse drug reactions: a comprehensive and clinical review.
        Clin Rev Allergy Immunol. 2015; 48: 165-175https://doi.org/10.1007/s12016-014-8418-y
        • Moher D.
        • Liberati A.
        • Tetzlaff J.
        • Altman D.G.
        Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
        BMJ. 2009; 339: b2535
        • Sohani Z.N.
        • Sarma S.
        • Alyass A.
        • de Souza R.J.
        • Robiou-du-Pont S.
        • Li A.
        • et al.
        Empirical evaluation of the Q-Genie tool: a protocol for assessment of effectiveness.
        BMJ Open. 2016; 6e010403https://doi.org/10.1136/bmjopen-2015-010403
      1. Centre T.N.C. Review Manager 5.3. 5.3 ed. UK: the Cochrane Collaboration; 2014.

        • Higgins J.P.
        • Thomas J.
        • Chandler J.
        • Cumpston M.
        • Li T.
        • Page M.J.
        • et al.
        Cochrane handbook for systematic reviews of interventions.
        John Wiley & Sons, 2019
      2. Borenstein M. Comprehensive meta-analysis software. Systematic Reviews in Health Research: meta-Analysis in Context. 2022:535–48.

      3. Sterne J., Egger M., Moher D.J., Afwhco. Chapter 10: addressing reporting biases in: Higgins JPT, Green S, editors. Cochrane handbook for systematic reviews of interventions. 2008.

        • Yuliwulandari R.
        • Kristin E.
        • Prayuni K.
        • Sachrowardi Q.
        • Suyatna F.D.
        • Menaldi S.L.
        • et al.
        Association of the HLA-B alleles with carbamazepine-induced Stevens–Johnson syndrome/toxic epidermal necrolysis in the Javanese and Sundanese population of Indonesia: the important role of the HLA-B75 serotype.
        Pharmacogenomics. 2017; 18: 1643-1648https://doi.org/10.2217/pgs-2017-0103
        • Nguyen K.D.
        • Tran T.N.
        • Nguyen M.T.
        • Nguyen H.A.
        • Nguyen Jr, H.A.
        • Vu D.H.
        • et al.
        Drug-induced Stevens–Johnson syndrome and toxic epidermal necrolysis in vietnamese spontaneous adverse drug reaction database: a subgroup approach to disproportionality analysis.
        J Clin Pharm Ther. 2019; 44: 69-77https://doi.org/10.1111/jcpt.12754
        • Kwan P.K.
        • Ng M.H.
        • Lo S.V.
        Association between HLA-B*15:02 allele and antiepileptic drug-induced severe cutaneous reactions in Hong Kong Chinese: a population-based study.
        Hong Kong Med J. 2014; 20 (Suppl): 16-18
        • He X.J.
        • Jian L.Y.
        • He X.L.
        • Wu Y.
        • Xu Y.Y.
        • Sun X.J.
        • et al.
        Association between the HLA-B*15:02 allele and carbamazepine-induced Stevens–Johnson syndrome/toxic epidermal necrolysis in Han individuals of northeastern China.
        Pharmacol Res. 2013; 65: 1256-1262https://doi.org/10.1016/s1734-1140(13)71483-x
        • Cheung Y.K.
        • Cheng S.H.
        • Chan E.J.
        • Lo S.V.
        • Ng M.H.
        • Kwan P.
        HLA-B alleles associated with severe cutaneous reactions to antiepileptic drugs in Han Chinese.
        Epilepsia. 2013; 54: 1307-1314https://doi.org/10.1111/epi.12217
        • Amstutz U.
        • Ross C.J.
        • Castro-Pastrana L.I.
        • Rieder M.J.
        • Shear N.H.
        • Hayden M.R.
        • et al.
        HLA-A 31:01 and HLA-B 15:02 as genetic markers for carbamazepine hypersensitivity in children.
        Clin Pharm Ther. 2013; 94: 142-149https://doi.org/10.1038/clpt.2013.55
        • Shi Y.W.
        • Min F.L.
        • Qin B.
        • Zou X.
        • Liu X.R.
        • Gao M.M.
        • et al.
        Association between HLA and Stevens–Johnson syndrome induced by carbamazepine in Southern Han Chinese: genetic markers besides B*1502?.
        Basic Clin Pharmacol Toxicol. 2012; 111: 58-64https://doi.org/10.1111/j.1742-7843.2012.00868.x
        • Niihara H.
        • Kaneko S.
        • Ito T.
        • Sugamori T.
        • Takahashi N.
        • Kohno K.
        • et al.
        HLA-B*58:01 strongly associates with allopurinol-induced adverse drug reactions in a Japanese sample population.
        J Dermatol Sci. 2013; 71: 150-152https://doi.org/10.1016/j.jdermsci.2013.04.013
        • Tassaneeyakul W.
        • Tiamkao S.
        • Jantararoungtong T.
        • Chen P.
        • Lin S.Y.
        • Chen W.H.
        • et al.
        Association between HLA-B*1502 and carbamazepine-induced severe cutaneous adverse drug reactions in a Thai population.
        Epilepsia. 2010; 51: 926-930https://doi.org/10.1111/j.1528-1167.2010.02533.x
        • Khor A.H.
        • Lim K.S.
        • Tan C.T.
        • Wong S.M.
        • Ng C.C.
        HLA-B*15:02 association with carbamazepine-induced Stevens–Johnson syndrome and toxic epidermal necrolysis in an Indian population: a pooled-data analysis and meta-analysis.
        Epilepsia. 2014; 55: e120-e124https://doi.org/10.1111/epi.12802
        • Locharernkul C.
        • Loplumlert J.
        • Limotai C.
        • Korkij W.
        • Desudchit T.
        • Tongkobpetch S.
        • et al.
        Carbamazepine and phenytoin induced Stevens–Johnson syndrome is associated with HLA-B*1502 allele in Thai population.
        Epilepsia. 2008; 49: 2087-2091https://doi.org/10.1111/j.1528-1167.2008.01719.x
        • Yampayon K.
        • Sukasem C.
        • Limwongse C.
        • Chinvarun Y.
        • Tempark T.
        • Rerkpattanapipat T.
        • et al.
        Influence of genetic and non-genetic factors on phenytoin-induced severe cutaneous adverse drug reactions.
        Eur J Clin Pharmacol. 2017; 73: 855-865https://doi.org/10.1007/s00228-017-2250-2
        • Manuyakorn W.
        • Mahasirimongkol S.
        • Likkasittipan P.
        • Kamchaisatian W.
        • Wattanapokayakit S.
        • Inunchot W.
        • et al.
        Association of HLA genotypes with phenobarbital hypersensitivity in children.
        Epilepsia. 2016; 57: 1610-1616https://doi.org/10.1111/epi.13509
        • Tassaneeyakul W.
        • Prabmeechai N.
        • Sukasem C.
        • Kongpan T.
        • Konyoung P.
        • Chumworathayi P.
        • et al.
        Associations between HLA class I and cytochrome P450 2C9 genetic polymorphisms and phenytoin-related severe cutaneous adverse reactions in a Thai population.
        Pharmacogenet Genom. 2016; 26: 225-234https://doi.org/10.1097/FPC.0000000000000211
        • Chang C.C.
        • Ng C.C.
        • Too C.L.
        • Choon S.E.
        • Lee C.K.
        • Chung W.H.
        • et al.
        Association of HLA-B*15:13 and HLA-B*15:02 with phenytoin-induced severe cutaneous adverse reactions in a Malay population.
        Pharmacogenomics J. 2017; 17: 170-173https://doi.org/10.1038/tpj.2016.10
        • Khor A.H.
        • Lim K.S.
        • Tan C.T.
        • Kwan Z.
        • Tan W.C.
        • Wu D.B.
        • et al.
        HLA-A*31: 01 and HLA-B*15:02 association with Stevens–Johnson syndrome and toxic epidermal necrolysis to carbamazepine in a multiethnic Malaysian population.
        Pharmacogenet Genom. 2017; 27: 275-278https://doi.org/10.1097/FPC.0000000000000287
        • Chang C.C.
        • Too C.L.
        • Murad S.
        • Hussein S.H.
        Association of HLA-B*1502 allele with carbamazepine-induced toxic epidermal necrolysis and Stevens–Johnson syndrome in the multi-ethnic Malaysian population.
        Int J Dermatol. 2011; 50: 221-224https://doi.org/10.1111/j.1365-4632.2010.04745.x
        • Hung S.I.
        • Chung W.H.
        • Liu Z.S.
        • Chen C.H.
        • Hsih M.S.
        • Hui R.C.
        • et al.
        Common risk allele in aromatic antiepileptic-drug induced Stevens–Johnson syndrome and toxic epidermal necrolysis in Han Chinese.
        Pharmacogenomics. 2010; 11: 349-356https://doi.org/10.2217/pgs.09.162
        • Wang W.
        • Hu F.Y.
        • Wu X.T.
        • An D.M.
        • Yan B.
        • Zhou D
        Genetic predictors of Stevens–Johnson syndrome and toxic epidermal necrolysis induced by aromatic antiepileptic drugs among the Chinese Han population.
        Epilepsy Behav. 2014; 37: 16-19https://doi.org/10.1016/j.yebeh.2014.05.025
        • Kaniwa N.
        • Sugiyama E.
        • Saito Y.
        • Kurose K.
        • Maekawa K.
        • Hasegawa R.
        • et al.
        Japan Pharmacogenomics Data Science Consortium. Specific HLA types are associated with antiepileptic drug-induced Stevens–Johnson syndrome and toxic epidermal necrolysis in Japanese subjects.
        Pharmacogenomics. 2013; 14: 1821-1831https://doi.org/10.2217/pgs.13.180
        • Capule F.
        • Tragulpiankit P.
        • Mahasirimongkol S.
        • Jittikoon J.
        • Wichukchinda N.
        • LT Alentajan-Aleta
        • et al.
        HLA-A*24:07 as a potential biomarker for carbamazepine-induced Stevens–Johnson syndrome/toxic epidermal necrolysis in Filipino patients.
        Pharmacogenomics. 2021; 22: 465-472https://doi.org/10.2217/pgs-2020-0191
        • John S.
        • Balakrishnan K.
        • Sukasem C.
        • Anand T.C.V.
        • Canyuk B.
        • Pattharachayakul S.
        Association of HLA-B*51:01, HLA-B*55:01, CYP2C9*3, and phenytoin-induced cutaneous adverse drug reactions in the South Indian Tamil population.
        J Pers Med. 2021; 11: 737https://doi.org/10.3390/jpm11080737
        • van Nguyen D.
        • Chu H.C.
        • Vidal C.
        • Fulton R.B.
        • Nguyen N.N.
        • Quynh Do N.T.
        • et al.
        Genetic susceptibilities and prediction modeling of carbamazepine and allopurinol-induced severe cutaneous adverse reactions in Vietnamese.
        Pharmacogenomics. 2021; 22: 1-12https://doi.org/10.2217/pgs-2019-0146
        • Mortazavi H.
        • Rostami A.
        • Firooz A.
        • Esmaili N.
        • Ghiasi M.
        • Lajevardi V.
        • et al.
        Association between human leukocyte antigens and cutaneous adverse drug reactions to antiepileptics and antibiotics in the Iranian population.
        Dermatol Ther. 2022; 35: e15393https://doi.org/10.1111/dth.15393
        • Huyen T.T.
        • Hoa P.D.
        • Trang T.M.
        • Khanh N.B.
        • Que T.N.
        • Phuong N.H.
        • et al.
        The link between HLA-B alleles and causative drugs in Vietnamese patients with Stevens–Johnson syndrome/toxic epidermal necrolysis.
        Open Access Maced J Med Sci. 2020; 8: 395-400https://doi.org/10.3889/oamjms.2020.4906
        • Mockenhaupt M.
        • Wang C.W.
        • Hung S.I.
        • Sekula P.
        • Schmidt A.H.
        • Pan R.Y.
        • et al.
        RegiSCAR group. HLA-B*57:01 confers genetic susceptibility to carbamazepine-induced SJS/TEN in Europeans.
        Allergy. 2019; 74: 2227-2230https://doi.org/10.1111/all.13821
        • Capule F.
        • Tragulpiankit P.
        • Mahasirimongkol S.
        • Jittikoon J.
        • Wichukchinda N.
        • Theresa Alentajan-Aleta L.
        • et al.
        Association of carbamazepine-induced Stevens–Johnson syndrome/toxic epidermal necrolysis with the HLA-B75 serotype or HLA-B*15:21 allele in Filipino patients.
        Pharmacogenomics J. 2020; 20: 533-541https://doi.org/10.1038/s41397-019-0143-8
        • Manuyakorn W.
        • Likkasittipan P.
        • Wattanapokayakit S.
        • Suvichapanich S.
        • Inunchot W.
        • Wichukchinda N.
        • et al.
        Association of HLA genotypes with phenytoin induced severe cutaneous adverse drug reactions in Thai children.
        Epilepsy Res. 2020; 162106321https://doi.org/10.1016/j.eplepsyres.2020.106321
        • Sabourirad S.
        • Mortezaee R.
        • Mojarad M.
        • Eslahi A.
        • Shahrokhi Y.
        • Kiafar B.
        • et al.
        Investigating the association of lamotrigine and phenytoin-induced Stevens–Johnson syndrome/toxic epidermal necrolysis with HLA-B*1502 in Iranian population.
        Exp Dermatol. 2021; 30: 284-287https://doi.org/10.1111/exd.14240
        • Nakkam N.
        • Konyoung P.
        • Amornpinyo W.
        • Saksit N.
        • Tiamkao S.
        • Khunarkornsiri U.
        • et al.
        Genetic variants associated with severe cutaneous adverse drug reactions induced by carbamazepine.
        Br J Clin Pharmacol. 2022; 88: 773-786https://doi.org/10.1111/bcp.15022
        • Man C.B.
        • Kwan P.
        • Baum L.
        • Yu E.
        • Lau K.M.
        • Cheng A.S.
        • et al.
        Association between HLA-B*1502 allele and antiepileptic drug-induced cutaneous reactions in Han Chinese.
        Epilepsia. 2007; 48: 1015-1018https://doi.org/10.1111/j.1528-1167.2007.01022.x
        • Haroon A.
        • Tripathi M.
        • Khanam R.
        • Vohora D.
        Antiepileptic drugs prescription utilization behavior and direct costs of treatment in a national hospital of India.
        Ann Indian Acad Neruol. 2012; 15: 289-293https://doi.org/10.4103/0972-2327.104338
        • Spina E.
        • Perugi G.
        Antiepileptic drugs: indications other than epilepsy.
        Epileptic Disord. 2004; 6: 57-75
        • Hanssens Y.
        • Deleu D.
        • Al Balushi K.
        • Al Hashar A.
        • Al-Zakwani I
        Drug utilization pattern of anti-epileptic drugs: a pharmacoepidemiologic study in Oman.
        J Clin Pharm Ther. 2002; 27: 357-364https://doi.org/10.1046/j.1365-2710.2002.00429.x
        • Carpio A.
        • Hauser W.A.
        Epilepsy in the developing world.
        Curr Neurol Neurosci Res. 2009; 9: 319-326https://doi.org/10.1007/s11910-009-0048-z
        • Trivedi B.S.
        • Darji N.H.
        • Malhotra S.D.
        • Patel P.R.
        Antiepileptic drugs-induced Stevens–Johnson syndrome: a case Series.
        J Basic Clin Pharmacol. 2016; 8: 42-44https://doi.org/10.4103/0976-0105.195130
        • Lonjou C.
        • Thomas L.
        • Borot N.
        • Ledger N.
        • de Toma C.
        • LeLouet H.
        • et al.
        A marker for Stevens–Johnson syndrome...: ethnicity matters.
        Pharmacogenomics J. 2006; 6: 265-268https://doi.org/10.1038/sj.tpj.6500356
        • Hung S.I.
        • Chung W.H.
        • Jee S.H.
        • Chen W.C.
        • Chang Y.T.
        • Lee W.R.
        • et al.
        Genetic susceptibility to carbamazepine-induced cutaneous adverse drug reactions.
        Pharmacogenet Genom. 2006; 16: 297-306https://doi.org/10.1097/01.fpc.0000199500.46842.4a
        • Hu F.-.Y.
        • Wu X.-.T.
        • An D-M
        • Yan B.
        • Stefan H.
        • Zhou D.
        Phenytoin-induced Stevens–Johnson syndrome with negative HLA-B*1502 allele in mainland China: two cases.
        Seizure. 2011; 20: 431-432https://doi.org/10.1016/j.seizure.2011.01.005
        • Vivar K.L.
        • Mancl K.
        • Seminario-Vidal L.
        Stevens–Johnson syndrome/toxic epidermal necrolysis associated with zonisamide.
        Clin Case Rep. 2017; 6: 258-261https://doi.org/10.1002/ccr3.1288
        • Manson L.E.N.
        • Swen J.J.
        • Guchelaar H.J.
        Diagnostic test criteria for HLA genotyping to prevent drug hypersensitivity reactions: a systematic review of actionable HLA recommendations in CPIC and DPWG guidelines.
        Front Pharmacol. 2020; 11567048https://doi.org/10.3389/fphar.2020.567048