Drug-Induced liver Injury Associated with Severe Cutaneous Hypersensitivity Reactions: A Complex Entity in Need of a Multidisciplinary Approach

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Abstract

Idiosyncratic drug-induced liver injury (DILI) occasionally occurs in the setting of severe cutaneous adverse reactions (SCARs), including Stevens-Johnson syndrome (SJS), toxic epidermal necrolysis (TEN) and drug reaction with eosinophilia and systemic symptoms (DRESS). This strengthens the proposed immunologic mechanism associated with this adverse reaction. DRESS exhibits the most common association with DILI. SCARs have a wide spectrum of heterogeneous clinical presentations and severity, and genetic predisposition has been identified. In the context of SCARs, DILI present a different clinical picture, ranging from mild injury to acute liver failure. Elucidating the role of DILI in the clinical presentation and outcome of SCARs represents a challenge due to limited information from published studies and the lack of consensus on definitions. The cholestatic and mixed pattern of liver damage typically predominates in the case of DILI associated with SCARs, which is different from DILI without SCARs where hepatocellular is the most common injury pattern. Only a few drugs have been associated with both DILI and SCARs. Is this article, the criteria used for DILI recognition among SCARS have been revised and discussed, along with the drugs most commonly involved in these syndromes as well as the outcome, prognostic factors and the need for a multidisciplinary approach to improve the management of DILI in the context of SCARs.

Keywords: Drug-induced liver injury, severe cutaneous adverse reactions, toxic epidermal necrolysis, liver injury, hypersensitivity reactions, hepatocellular.

[1]
Stephens C, Andrade RJ. Genetic predisposition to drug-induced liver injury. Clin Liver Dis 2019; In press.
[2]
Dara L, Liu Z-X, Kaplowitz N. Mechanisms of adaptation and progression in idiosyncratic drug induced liver injury, clinical implications. Liver Int 2016; 36(2): 158-65.
[http://dx.doi.org/10.1111/liv.12988] [PMID: 26484420]
[3]
Chalasani N, Bonkovsky HL, Fontana R, et al. Features and outcomes of 899 patients with drug-induced liver injury: the DILIN prospective study. Gastroenterology 2015. 148(7): 1340-52: e7.
[http://dx.doi.org/10.1053/j.gastro.2015.03.006] [PMID: 25754159]
[4]
Andrade RJ, Lucena MI, Fernández MC, et al. Drug-induced liver injury: an analysis of 461 incidences submitted to the spanish registry over a 10-year period. Gastroenterology 2005; 129(2): 512-21.
[http://dx.doi.org/10.1016/j.gastro.2005.05.006] [PMID: 16083708]
[5]
Kullak-Ublick GA, Andrade RJ, Merz M, et al. Drug-induced liver injury: recent advances in diagnosis and risk assessment. Gut 2017; 66(6): 1154-64.
[http://dx.doi.org/10.1136/gutjnl-2016-313369] [PMID: 28341748]
[6]
Devarbhavi H, Dierkhising R, Kremers WK, Sandeep MS, Karanth D, Adarsh CK. Single-center experience with drug-induced liver injury from India: causes, outcome, prognosis, and predictors of mortality. Am J Gastroenterol 2010; 105(11): 2396-404.
[http://dx.doi.org/10.1038/ajg.2010.287] [PMID: 20648003]
[7]
Karnes JH, Miller MA, White KD, et al. Applications of immunopharmacogenomics: predicting, preventing, and understanding immune-mediated adverse drug reactions. Annu Rev Pharmacol Toxicol 2019; 59: 463-86.
[http://dx.doi.org/10.1146/annurev-pharmtox-010818-021818] [PMID: 30134124]
[8]
Kaliyaperumal K, Grove JI, Delahay RM, Griffiths WJH, Duckworth A, Aithal GP. Pharmacogenomics of drug-induced liver injury (DILI): molecular biology to clinical applications. J Hepatol 2018; 69(4): 948-57.
[http://dx.doi.org/10.1016/j.jhep.2018.05.013] [PMID: 29792895]
[9]
Sousa-Pinto B, Correia C, Gomes L, et al. HLA and delayed drug-induced hypersensitivity. Int Arch Allergy Immunol 2016; 170(3): 163-79.
[http://dx.doi.org/10.1159/000448217] [PMID: 27576480]
[10]
Nicoletti P, Barrett S, McEvoy L, et al. Shared genetic risk factors across carbamazepine‐induced hypersensitivity reactions. Clin Pharmacol Ther 2019; 106(5): 1028-36.
[http://dx.doi.org/10.1002/cpt.1493] [PMID: 31066027]
[11]
Fang WC, Adler NR, Graudins LV, et al. Drug-induced liver injury is frequently associated with severe cutaneous adverse drug reactions: experience from two australian tertiary hospitals. Intern Med J 2018; 48(5): 549-55.
[http://dx.doi.org/10.1111/imj.13734] [PMID: 29316113]
[12]
Lee T, Lee YS, Yoon S-Y, et al. Characteristics of liver injury in drug-induced systemic hypersensitivity reactions. J Am Acad Dermatol 2013; 69(3): 407-15.
[http://dx.doi.org/10.1016/j.jaad.2013.03.024] [PMID: 23632341]
[13]
Lin I-C, Yang H-C, Strong C, et al. Liver injury in patients with DRESS: a clinical study of 72 cases. J Am Acad Dermatol 2015; 72(6): 984-91.
[http://dx.doi.org/10.1016/j.jaad.2015.02.1130] [PMID: 25801338]
[14]
Bastuji-Garin S, Fouchard N, Bertocchi M, Roujeau JC, Revuz J, Wolkenstein P. SCORTEN: a severity-of-illness score for toxic epidermal necrolysis. J Invest Dermatol 2000; 115(2): 149-53.
[http://dx.doi.org/10.1046/j.1523-1747.2000.00061.x] [PMID: 10951229]
[15]
French LE. Toxic epidermal necrolysis and stevens-johnson syndrome: our current understanding. Allergol Int 2006; 55(1): 9-16.
[http://dx.doi.org/10.2332/allergolint.55.9] [PMID: 17075281]
[16]
Pirmohamed M, Friedmann PS, Molokhia M, et al. Phenotype standardization for immune-mediated drug-induced skin injury. Clin Pharmacol Ther 2011; 89(6): 896-901.
[http://dx.doi.org/10.1038/clpt.2011.79] [PMID: 21562486]
[17]
Lerch M, Mainetti C, Terziroli Beretta-Piccoli B, Harr T. Current perspectives on stevens-johnson syndrome and toxic epidermal necrolysis. Clin Rev Allergy Immunol 2018; 54(1): 147-76.
[http://dx.doi.org/10.1007/s12016-017-8654-z] [PMID: 29188475]
[18]
Kardaun SH, Sekula P, Valeyrie-Allanore L, et al. Drug reaction with eosinophilia and systemic symptoms (DRESS): an original multisystem adverse drug reaction. Results from the prospective RegiSCAR study. Br J Dermatol 2013; 169(5): 1071-80.
[http://dx.doi.org/10.1111/bjd.12501] [PMID: 23855313]
[19]
De A, Rajagopalan M, Sarda A, Das S, Biswas P. Drug reaction with eosinophilia and systemic symptoms: an update and review of recent literature. Indian J Dermatol 2018; 63(1): 30-40.
[http://dx.doi.org/10.4103/ijd.IJD_582_17] [PMID: 29527023]
[20]
Aithal GP, Watkins PB, Andrade RJ, et al. Case definition and phenotype standardization in drug-induced liver injury. Clin Pharmacol Ther 2011; 89(6): 806-15.
[http://dx.doi.org/10.1038/clpt.2011.58] [PMID: 21544079]
[21]
Andrade RJ, Aithal GP, Björnsson ES, et al. EASL Clinical practice guidelines: drug-induced liver injury. J Hepatol 2019; 70(6): 1222-61.
[http://dx.doi.org/10.1016/j.jhep.2019.02.014]
[22]
Medina-Caliz I, Almarza M, Stephens C, et al. DRESS cases included in the spanish and latin-american DILI registries: clinical phenotype and outcome. J Hepatol 2018; 68(Suppl. 1): S601.
[http://dx.doi.org/10.1016/S0168-8278(18)31459-4]
[23]
Skowron F, Bensaid B, Balme B, et al. Drug reaction with eosinophilia and systemic symptoms (DRESS): clinicopathological study of 45 cases. J Eur Acad Dermatol Venereol 2015; 29(11): 2199-205.
[http://dx.doi.org/10.1111/jdv.13212] [PMID: 26354734]
[24]
Chen Y-C, Chiu H-C, Chu C-Y. Drug reaction with eosinophilia and systemic symptoms: a retrospective study of 60 cases. Arch Dermatol 2010; 146(12): 1373-9.
[http://dx.doi.org/10.1001/archdermatol.2010.198] [PMID: 20713773]
[25]
Su P, Aw CWD. Severe cutaneous adverse reactions in a local hospital setting: a 5-year retrospective study. Int J Dermatol 2014; 53(11): 1339-45.
[http://dx.doi.org/10.1111/ijd.12118] [PMID: 25070588]
[26]
Han XD, Koh MJ-A, Wong SMY. Drug reaction with eosinophilia and systemic symptoms in a cohort of Asian children. Pediatr Dermatol 2019; 36(3): 324-9.
[http://dx.doi.org/10.1111/pde.13812] [PMID: 30920020]
[27]
Hiransuthikul A, Rattananupong T, Klaewsongkram J, Rerknimitr P, Pongprutthipan M, Ruxrungtham K. Drug-induced hypersensitivity syndrome/drug reaction with eosinophilia and systemic symptoms (DIHS/DRESS): 11 years retrospective study in Thailand. Allergol Int 2016; 65(4): 432-8.
[http://dx.doi.org/10.1016/j.alit.2016.04.001] [PMID: 27134114]
[28]
Walsh S, Diaz-Cano S, Higgins E, et al. Drug reaction with eosinophilia and systemic symptoms: is cutaneous phenotype a prognostic marker for outcome? A review of clinicopathological features of 27 cases. Br J Dermatol 2013; 168(2): 391-401.
[http://dx.doi.org/10.1111/bjd.12081] [PMID: 23034060]
[29]
Devarbhavi H, Raj S, Aradya VH, et al. Drug-induced liver injury associated with stevens-johnson syndrome/toxic epidermal necrolysis: patient characteristics, causes, and outcome in 36 cases. Hepatology 2016; 63(3): 993-9.
[http://dx.doi.org/10.1002/hep.28270] [PMID: 26439084]
[30]
Sassolas B, Haddad C, Mockenhaupt M, et al. ALDEN, an algorithm for assessment of drug causality in stevens-johnson syndrome and toxic epidermal necrolysis: comparison with case-control analysis. Clin Pharmacol Ther 2010; 88(1): 60-8.
[http://dx.doi.org/10.1038/clpt.2009.252] [PMID: 20375998]
[31]
Goldman JL, Chung W-H, Lee BR, et al. Adverse drug reaction causality assessment tools for drug-induced stevens-johnson syndrome and toxic epidermal necrolysis: room for improvement. Eur J Clin Pharmacol 2019; 75(8): 1135-41.
[http://dx.doi.org/10.1007/s00228-019-02670-9]
[32]
García-Cortés M, Stephens C, Lucena MI, Fernández-Castañer A, Andrade RJ. Causality assessment methods in drug induced liver injury: strengths and weaknesses. J Hepatol 2011; 55(3): 683-91.
[http://dx.doi.org/10.1016/j.jhep.2011.02.007] [PMID: 21349301]
[33]
García-Cortés M, Lucena MI, Pachkoria K, Borraz Y, Hidalgo R, Andrade RJ. Evaluation of naranjo adverse drug reactions probability scale in causality assessment of drug-induced liver injury. Aliment Pharmacol Ther 2008; 27(9): 780-9.
[http://dx.doi.org/10.1111/j.1365-2036.2008.03655.x] [PMID: 18284654]
[34]
Ang C-C, Wang Y-S, Yoosuff E-LM, Tay Y-K. Retrospective analysis of drug-induced hypersensitivity syndrome: a study of 27 patients. J Am Acad Dermatol 2010; 63(2): 219-27.
[http://dx.doi.org/10.1016/j.jaad.2009.08.050] [PMID: 20605253]
[35]
Eshki M, Allanore L, Musette P, et al. Twelve-year analysis of severe cases of drug reaction with eosinophilia and systemic symptoms: a cause of unpredictable multiorgan failure. Arch Dermatol 2009; 145(1): 67-72.
[http://dx.doi.org/10.1001/archderm.145.1.67] [PMID: 19153346]
[36]
Zhang F-R, Liu H, Irwanto A, et al. HLA-B*13:01 and the dapsone hypersensitivity syndrome. N Engl J Med 2013; 369(17): 1620-8.
[http://dx.doi.org/10.1056/NEJMoa1213096] [PMID: 24152261]
[37]
Chen Y-C, Cho Y-T, Chang C-Y, Chu C-Y. Drug reaction with eosinophilia and systemic symptoms: a drug-induced hypersensitivity syndrome with variable clinical features. Dermatologica Sin 2013; 31: 196-204.
[http://dx.doi.org/10.1016/j.dsi.2013.09.006]
[38]
Björnsson ES, Bergmann OM, Björnsson HK, Kvaran RB, Olafsson S. Incidence, presentation, and outcomes in patients with drug-induced liver injury in the general population of iceland. Gastroenterology 2013; 144(7): 1419-25.
[http://dx.doi.org/10.1053/j.gastro.2013.02.006] [PMID: 23419359]
[39]
Lucena MI, Andrade RJ, Kaplowitz N, et al. Phenotypic characterization of idiosyncratic drug-induced liver injury: the influence of age and sex. Hepatology 2009; 49(6): 2001-9.
[http://dx.doi.org/10.1002/hep.22895] [PMID: 19475693]
[40]
Sim DW, Yu JE, Jeong J, et al. Variation of clinical manifestations according to culprit drugs in DRESS syndrome. Pharmacoepidemiol Drug Saf 2019; 28(6): 840-8.
[http://dx.doi.org/10.1002/pds.4774] [PMID: 31044478]
[41]
Andrade RJ, Lucena MI, Kaplowitz N, et al. Outcome of acute idiosyncratic drug-induced liver injury: long-term follow-up in a hepatotoxicity registry. Hepatology 2006; 44(6): 1581-8.
[http://dx.doi.org/10.1002/hep.21424] [PMID: 17133470]
[42]
Robles-Diaz M, Lucena MI, Kaplowitz N, et al. Use of Hy’s law and a new composite algorithm to predict acute liver failure in patients with drug-induced liver injury. Gastroenterology 2014. 147(1): 109-118: e5.
[http://dx.doi.org/10.1053/j.gastro.2014.03.050] [PMID: 24704526]
[43]
Ichai P, Laurent-Bellue A, Saliba F, et al. Acute liver failure/injury related to drug reaction with eosinophilia and systemic symptoms: outcomes and prognostic factors. Transplantation 2017; 101(8): 1830-7.
[http://dx.doi.org/10.1097/TP.0000000000001655] [PMID: 28207633]
[44]
Su S-C, Mockenhaupt M, Wolkenstein P, et al. Interleukin-15 is associated with severity and mortality in stevens-johnson syndrome/toxic epidermal necrolysis. J Invest Dermatol 2017; 137(5): 1065-73.
[http://dx.doi.org/10.1016/j.jid.2016.11.034] [PMID: 28011147]
[45]
Pachkoria K, Lucena MI, Crespo E, et al. Analysis of IL-10, IL-4 and TNF-alpha polymorphisms in drug-induced liver injury (DILI) and its outcome. J Hepatol 2008; 49(1): 107-14.
[http://dx.doi.org/10.1016/j.jhep.2008.03.017] [PMID: 18485518]
[46]
Kleiner DE, Chalasani NP, Lee WM, et al. Hepatic histological findings in suspected drug-induced liver injury: systematic evaluation and clinical associations. Hepatology 2014; 59(2): 661-70.
[http://dx.doi.org/10.1002/hep.26709] [PMID: 24037963]
[47]
Oh HL, Kang DY, Kang HR, et al. Severe cutaneous adverse reactions in korean pediatric patients: a study from the korea SCAR registry. Allergy Asthma Immunol Res 2019; 11(2): 241-53.
[http://dx.doi.org/10.4168/aair.2019.11.2.241] [PMID: 30661316]
[48]
Waldman R, Whitaker-Worth D, Grant-Kels JM. Cutaneous adverse drug reactions: kids are not just little people. Clin Dermatol 2017; 35(6): 566-82.
[http://dx.doi.org/10.1016/j.clindermatol.2017.08.007] [PMID: 29191348]
[49]
Levi N, Bastuji-Garin S, Mockenhaupt M, et al. Medications as risk factors of stevens-johnson syndrome and toxic epidermal necrolysis in children: a pooled analysis. Pediatrics 2009; 123(2): e297-304.
[http://dx.doi.org/10.1542/peds.2008-1923] [PMID: 19153164]
[50]
Illing PT, Purcell AW, McCluskey J. The role of HLA genes in pharmacogenomics: unravelling HLA associated adverse drug reactions. Immunogenetics 2017; 69(8-9): 617-30.
[http://dx.doi.org/10.1007/s00251-017-1007-5] [PMID: 28695285]
[51]
Romano A, Pettinato R, Andriolo M, et al. Hypersensitivity to aromatic anticonvulsants: in vivo and in vitro cross-reactivity studies. Curr Pharm Des 2006; 12(26): 3373-81.
[http://dx.doi.org/10.2174/138161206778193962] [PMID: 17017931]
[52]
Zgolli F, Aouinti I, Charfi O, et al. Drug rash with eosinophilia and systemic symptoms (DRESS) syndrome induced by imatinib. Curr Drug Saf 2019; 14(2): 151-4.
[http://dx.doi.org/10.2174/1574886314666190130150243] [PMID: 30706827]
[53]
Dyck L, Mills KHG. Immune checkpoints and their inhibition in cancer and infectious diseases. Eur J Immunol 2017; 47(5): 765-79.
[http://dx.doi.org/10.1002/eji.201646875] [PMID: 28393361]
[54]
Callahan MK, Postow MA, Wolchok JD, Targeting T. Targeting T cell co-receptors for cancer therapy. Immunity 2016; 44(5): 1069-78.
[http://dx.doi.org/10.1016/j.immuni.2016.04.023] [PMID: 27192570]
[55]
Mirza S, Hill E, Ludlow SP, Nanjappa S. Checkpoint inhibitor-associated drug reaction with eosinophilia and systemic symptom syndrome. Melanoma Res 2017; 27(3): 271-3.
[http://dx.doi.org/10.1097/CMR.0000000000000326] [PMID: 28146044]
[56]
Sanlorenzo M, Vujic I, Daud A, et al. Pembrolizumab cutaneous adverse events and their association with disease progression. JAMA Dermatol 2015; 151(11): 1206-12.
[http://dx.doi.org/10.1001/jamadermatol.2015.1916] [PMID: 26222619]
[57]
Chirasuthat P, Chayavichitsilp P. Atezolizumab-induced stevens-johnson syndrome in a patient with non-small cell lung carcinoma. Case Rep Dermatol 2018; 10(2): 198-202.
[http://dx.doi.org/10.1159/000492172] [PMID: 30186133]
[58]
Puzanov I, Diab A, Abdallah K, et al. Managing toxicities associated with immune checkpoint inhibitors: consensus recommendations from the Society for immunotherapy of cancer (SITC) toxicity management working group. J Immunother Cancer 2017; 5(1): 95.
[http://dx.doi.org/10.1186/s40425-017-0300-z] [PMID: 29162153]
[59]
Chen M, Suzuki A, Borlak J, Andrade RJ, Lucena MI. Drug-induced liver injury: interactions between drug properties and host factors. J Hepatol 2015; 63(2): 503-14.
[http://dx.doi.org/10.1016/j.jhep.2015.04.016] [PMID: 25912521]
[60]
Naisbitt DJ, Britschgi M, Wong G, et al. Hypersensitivity reactions to carbamazepine: characterization of the specificity, phenotype, and cytokine profile of drug-specific T cell clones. Mol Pharmacol 2003; 63(3): 732-41.
[http://dx.doi.org/10.1124/mol.63.3.732] [PMID: 12606784]
[61]
Pichler WJ. Delayed drug hypersensitivity reactions. Ann Intern Med 2003; 139(8): 683-93.
[http://dx.doi.org/10.7326/0003-4819-139-8-200310210-00012] [PMID: 14568857]
[62]
Wu Y, Farrell J, Pirmohamed M, Park BK, Naisbitt DJ. Generation and characterization of antigen-specific CD4+, CD8+, and CD4+CD8+ T-cell clones from patients with carbamazepine hypersensitivity. J Allergy Clin Immunol 2007; 119(4): 973-81.
[http://dx.doi.org/10.1016/j.jaci.2006.12.617] [PMID: 17320939]
[63]
Morel E, Escamochero S, Cabañas R, Díaz R, Fiandor A, Bellón T. CD94/NKG2C is a killer effector molecule in patients with stevens- johnson syndrome and toxic epidermal necrolysis. J Allergy Clin Immunol 2010; 125: 703-10, 710.e1-710.e8.
[64]
Nassif A, Bensussan A, Boumsell L, et al. Toxic epidermal necrolysis: effector cells are drug-specific cytotoxic T cells. J Allergy Clin Immunol 2004; 114(5): 1209-15.
[http://dx.doi.org/10.1016/j.jaci.2004.07.047] [PMID: 15536433]
[65]
Grove JI, Aithal GP. Human leukocyte antigen genetic risk factors of drug-induced liver toxicology. Expert Opin Drug Metab Toxicol 2015; 11(3): 395-409.
[http://dx.doi.org/10.1517/17425255.2015.992414] [PMID: 25491399]
[66]
White KD, Chung W-H, Hung S-I, Mallal S, Phillips EJ. Evolving models of the immunopathogenesis of T cell-mediated drug allergy: The role of host, pathogens, and drug response. J Allergy Clin Immunol 2015; 136(2): 219-34.
[http://dx.doi.org/10.1016/j.jaci.2015.05.050] [PMID: 26254049]
[67]
Hung S-I, Chung W-H, Liou L-B, et al. HLA-B*5801 allele as a genetic marker for severe cutaneous adverse reactions caused by allopurinol. Proc Natl Acad Sci USA 2005; 102(11): 4134-9.
[http://dx.doi.org/10.1073/pnas.0409500102] [PMID: 15743917]
[68]
Gonçalo M, Coutinho I, Teixeira V, et al. HLA-B*58:01 is a risk factor for allopurinol-induced DRESS and stevens-johnson syndrome/toxic epidermal necrolysis in a portuguese population. Br J Dermatol 2013; 169(3): 660-5.
[http://dx.doi.org/10.1111/bjd.12389] [PMID: 23600531]
[69]
Tassaneeyakul W, Jantararoungtong T, Chen P, et al. Strong association between HLA-B*5801 and allopurinol-induced stevens-johnson syndrome and toxic epidermal necrolysis in a thai population. Pharmacogenet Genomics 2009; 19(9): 704-9.
[http://dx.doi.org/10.1097/FPC.0b013e328330a3b8] [PMID: 19696695]
[70]
Ozeki T, Mushiroda T, Yowang A, et al. Genome-wide association study identifies HLA-A*3101 allele as a genetic risk factor for carbamazepine-induced cutaneous adverse drug reactions in Japanese population. Hum Mol Genet 2011; 20(5): 1034-41.
[http://dx.doi.org/10.1093/hmg/ddq537] [PMID: 21149285]
[71]
McCormack M, Alfirevic A, Bourgeois S, et al. HLA-A*3101 and carbamazepine-induced hypersensitivity reactions in Europeans. N Engl J Med 2011; 364(12): 1134-43.
[http://dx.doi.org/10.1056/NEJMoa1013297] [PMID: 21428769]
[72]
Chung W-H, Hung S-I, Hong H-S, et al. Medical genetics: a marker for stevens-johnson syndrome. Nature 2004; 428(6982): 486-6.
[http://dx.doi.org/10.1038/428486a] [PMID: 15057820]
[73]
Chang C-C, Too C-L, Murad S, Hussein SH. 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(2): 221-4.
[http://dx.doi.org/10.1111/j.1365-4632.2010.04745.x] [PMID: 21244392]
[74]
Locharernkul C, Loplumlert J, Limotai C, et al. Carbamazepine and phenytoin induced stevens-johnson syndrome is associated with HLA-B*1502 allele in thai population. Epilepsia 2008; 49(12): 2087-91.
[http://dx.doi.org/10.1111/j.1528-1167.2008.01719.x] [PMID: 18637831]
[75]
Kim S-H, Lee KW, Song W-J, et al. Carbamazepine-induced severe cutaneous adverse reactions and HLA genotypes in koreans. Epilepsy Res 2011; 97(1-2): 190-7.
[http://dx.doi.org/10.1016/j.eplepsyres.2011.08.010] [PMID: 21917426]
[76]
Hung S-I, Chung W-H, Liu Z-S, et al. Common risk allele in aromatic antiepileptic-drug induced stevens-johnson syndrome and toxic epidermal necrolysis in Han Chinese. Pharmacogenomics 2010; 11(3): 349-56.
[http://dx.doi.org/10.2217/pgs.09.162] [PMID: 20235791]
[77]
Cheung Y-K, Cheng S-H, Chan EJM, Lo SV, Ng MHL, Kwan P. HLA-B alleles associated with severe cutaneous reactions to antiepileptic drugs in han chinese. Epilepsia 2013; 54(7): 1307-14.
[http://dx.doi.org/10.1111/epi.12217] [PMID: 23692434]
[78]
Yang F, Gu B, Zhang L, et al. HLA-B*13:01 is associated with salazosulfapyridine-induced drug rash with eosinophilia and systemic symptoms in Chinese Han population. Pharmacogenomics 2014; 15(11): 1461-9.
[http://dx.doi.org/10.2217/pgs.14.69] [PMID: 25303297]
[79]
Lucena MI, Molokhia M, Shen Y, et al. Susceptibility to amoxicillin-clavulanate-induced liver injury is influenced by multiple HLA class I and II alleles. Gastroenterology 2011; 141(1): 338-47.
[http://dx.doi.org/10.1053/j.gastro.2011.04.001] [PMID: 21570397]
[80]
Singer JB, Lewitzky S, Leroy E, et al. A genome-wide study identifies HLA alleles associated with lumiracoxib-related liver injury. Nat Genet 2010; 42(8): 711-4.
[http://dx.doi.org/10.1038/ng.632] [PMID: 20639878]
[81]
Mallal S, Nolan D, Witt C, et al. Association between presence of HLA-B*5701, HLA-DR7, and HLA-DQ3 and hypersensitivity to HIV-1 reverse-transcriptase inhibitor abacavir. Lancet 2002; 359(9308): 727-32.
[http://dx.doi.org/10.1016/S0140-6736(02)07873-X] [PMID: 11888582]
[82]
Daly AK, Donaldson PT, Bhatnagar P, et al. HLA-B*5701 genotype is a major determinant of drug-induced liver injury due to flucloxacillin. Nat Genet 2009; 41(7): 816-9.
[http://dx.doi.org/10.1038/ng.379] [PMID: 19483685]
[83]
Xu C-F, Johnson T, Wang X, et al. HLA-B*57:01 confers susceptibility to pazopanib-associated liver injury in patients with cancer. Clin Cancer Res 2016; 22(6): 1371-7.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-2044] [PMID: 26546620]
[84]
Illing PT, Vivian JP, Dudek NL, et al. Immune self-reactivity triggered by drug-modified HLA-peptide repertoire. Nature 2012; 486(7404): 554-8.
[http://dx.doi.org/10.1038/nature11147] [PMID: 22722860]
[85]
Monshi MM, Faulkner L, Gibson A, et al. Human leukocyte antigen (HLA)-B*57:01-restricted activation of drug-specific T cells provides the immunological basis for flucloxacillin-induced liver injury. Hepatology 2013; 57(2): 727-39.
[http://dx.doi.org/10.1002/hep.26077] [PMID: 22987284]
[86]
Mallal S, Phillips E, Carosi G, et al. HLA-B*5701 screening for hypersensitivity to abacavir. N Engl J Med 2008; 358(6): 568-79.
[http://dx.doi.org/10.1056/NEJMoa0706135] [PMID: 18256392]
[87]
Yip VLM, Alfirevic A, Pirmohamed M. Genetics of immune-mediated adverse drug reactions: a comprehensive and clinical review. Clin Rev Allergy Immunol 2015; 48(2-3): 165-75.
[http://dx.doi.org/10.1007/s12016-014-8418-y] [PMID: 24777842]
[88]
Schackman BR, Scott CA, Walensky RP, Losina E, Freedberg KA, Sax PE. The cost-effectiveness of HLA-B*5701 genetic screening to guide initial antiretroviral therapy for HIV. AIDS 2008; 22(15): 2025-33.
[http://dx.doi.org/10.1097/QAD.0b013e3283103ce6] [PMID: 18784465]
[89]
Alfirevic A, Pirmohamed M. Predictive genetic testing for drug-induced liver injury: considerations of clinical utility. Clin Pharmacol Ther 2012; 92(3): 376-80.
[http://dx.doi.org/10.1038/clpt.2012.107] [PMID: 22850601]
[90]
Ferrell PB Jr, McLeod HL. Carbamazepine, HLA-B*1502 and risk of stevens-johnson syndrome and toxic epidermal necrolysis: US FDA recommendations. Pharmacogenomics 2008; 9(10): 1543-6.
[http://dx.doi.org/10.2217/14622416.9.10.1543] [PMID: 18855540]
[91]
Phillips EJ, Sukasem C, Whirl-Carrillo M, et al. Clinical pharmacogenetics implementation consortium guideline for HLA genotype and use of carbamazepine and oxcarbazepine. Clin Pharmacol Ther 2018; 103(4): 574-81.
[http://dx.doi.org/10.1002/cpt.1004] [PMID: 29392710]
[92]
Yip VLM, Pirmohamed M. The HLA-A*31:01 allele: influence on carbamazepine treatment. Pharm Genomics Pers Med 2017; 10: 29-38.
[http://dx.doi.org/10.2147/PGPM.S108598] [PMID: 28203102]
[93]
Shiohara T, Mizukawa Y. Drug-induced hypersensitivity syndrome (DiHS)/drug reaction with eosinophilia and systemic symptoms (DRESS): an update in 2019. Allergol Int 2019; 68(3): 301-8.
[http://dx.doi.org/10.1016/j.alit.2019.03.006] [PMID: 31000444]
[94]
Kano Y, Hiraharas K, Sakuma K, Shiohara T. Several herpesviruses can reactivate in a severe drug-induced multiorgan reaction in the same sequential order as in graft-versus-host disease. Br J Dermatol 2006; 155(2): 301-6.
[http://dx.doi.org/10.1111/j.1365-2133.2006.07238.x] [PMID: 16882166]
[95]
Tohyama M, Hashimoto K, Yasukawa M, et al. Association of human herpesvirus 6 reactivation with the flaring and severity of drug-induced hypersensitivity syndrome. Br J Dermatol 2007; 157(5): 934-40.
[http://dx.doi.org/10.1111/j.1365-2133.2007.08167.x] [PMID: 17854362]
[96]
Picard D, Janela B, Descamps V, et al. Drug reaction with eosinophilia and systemic symptoms (DRESS): a multiorgan antiviral T cell response. Sci Transl Med 2010; 2(46)46ra62
[http://dx.doi.org/10.1126/scitranslmed.3001116] [PMID: 20739682]
[97]
Seishima M, Yamanaka S, Fujisawa T, Tohyama M, Hashimoto K. Reactivation of human herpesvirus (HHV) family members other than HHV-6 in drug-induced hypersensitivity syndrome. Br J Dermatol 2006; 155(2): 344-9.
[http://dx.doi.org/10.1111/j.1365-2133.2006.07332.x] [PMID: 16882173]
[98]
Tetart F, Picard D, Janela B, Joly P, Musette P. Prolonged evolution of drug reaction with eosinophilia and systemic symptoms: clinical, virologic, and biological features. JAMA Dermatol 2014; 150(2): 206-7.
[http://dx.doi.org/10.1001/jamadermatol.2013.6698] [PMID: 24369386]
[99]
Medina-Cáliz I, Robles-Díaz M, Lucena MI, Andrade RJ. Drug-induced liver and skin reactions: in need of a consensus definition. Hepatology 2017; 65(1): 391.
[http://dx.doi.org/10.1002/hep.28808] [PMID: 27618725]
[100]
Sharma AM, Uetrecht J. Bioactivation of drugs in the skin: relationship to cutaneous adverse drug reactions. Drug Metab Rev 2014; 46(1): 1-18.
[http://dx.doi.org/10.3109/03602532.2013.848214] [PMID: 24164504]
[101]
Hirashima R, Itoh T, Tukey RH, Fujiwara R. Prediction of drug-induced liver injury using keratinocytes. J Appl Toxicol 2017; 37(7): 863-72.
[http://dx.doi.org/10.1002/jat.3435] [PMID: 28138970]
[102]
Shiohara T, Kano Y. Drug reaction with eosinophilia and systemic symptoms (DRESS): incidence, pathogenesis and management. Expert Opin Drug Saf 2017; 16(2): 139-47.
[PMID: 27936971]
[103]
Hetherington S, Hughes AR, Mosteller M, et al. Genetic variations in HLA-B region and hypersensitivity reactions to abacavir. Lancet 2002; 359(9312): 1121-2.
[http://dx.doi.org/10.1016/S0140-6736(02)08158-8] [PMID: 11943262]
[104]
Hughes AR, Mosteller M, Bansal AT, et al. Association of genetic variations in HLA-B region with hypersensitivity to abacavir in some, but not all, populations. Pharmacogenomics 2004; 5(2): 203-11.
[http://dx.doi.org/10.1517/phgs.5.2.203.27481] [PMID: 15016610]
[105]
Genin E, Chen D-P, Hung S-I, et al. HLA-A*31:01 and different types of carbamazepine-induced severe cutaneous adverse reactions: an international study and meta-analysis. Pharmacogenomics J 2014; 14(3): 281-8.
[http://dx.doi.org/10.1038/tpj.2013.40] [PMID: 24322785]
[106]
Tempark T, Satapornpong P, Rerknimitr P, et al. Dapsone-induced severe cutaneous adverse drug reactions are strongly linked with HLA-B*13: 01 allele in the thai population. Pharmacogenet Genomics 2017; 27(12): 429-37.
[http://dx.doi.org/10.1097/FPC.0000000000000306] [PMID: 28885988]
[107]
Ramírez E, Bellón T, Tong HY, 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: 168-78.
[http://dx.doi.org/10.1016/j.phrs.2016.11.027] [PMID: 27888155]
[108]
Yuan J, Guo S, Hall D, et al. Toxicogenomics of nevirapine-associated cutaneous and hepatic adverse events among populations of african, asian, and european descent. AIDS 2011; 25(10): 1271-80.
[http://dx.doi.org/10.1097/QAD.0b013e32834779df] [PMID: 21505298]
[109]
Vitezica ZG, Milpied B, Lonjou C, et al. HLA-DRB1*01 associated with cutaneous hypersensitivity induced by nevirapine and efavirenz. AIDS 2008; 22(4): 540-1.
[http://dx.doi.org/10.1097/QAD.0b013e3282f37812] [PMID: 18301070]
[110]
Sharma SK, Balamurugan A, Saha PK, Pandey RM, Mehra NK. Evaluation of clinical and immunogenetic risk factors for the development of hepatotoxicity during antituberculosis treatment. Am J Respir Crit Care Med 2002; 166(7): 916-9.
[http://dx.doi.org/10.1164/rccm.2108091] [PMID: 12359646]
[111]
Nicoletti P, Devarbhavi H, Goel A, Eapen CE, Venkatesan R, Grove JI, et al. Genome-wide association study (GWAS) to identify genetic risk factors that increase susceptibility to antituberculosis drug-induced liver injury (ATDILI). Hepatology 2017; 66(Suppl. 1): 25A.
[112]
Leiro-Fernández V, Valverde D, Vázquez-Gallardo R, Constenla-Caramés L, Del Campo-Pérez V, Fernández-Villar A. HLA-DQ B1*0201 and A1*0102 alleles are not responsible for antituberculosis drug-induced hepatotoxicity risk in spanish population. Front Med (Lausanne) 2016; 3: 34.
[http://dx.doi.org/10.3389/fmed.2016.00034] [PMID: 27597944]