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Review

HLA-associated Drug Hypersensitivity and the Prediction of Adverse Drug Reactions

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Pages 1441-1457 | Received 23 May 2017, Accepted 19 Jul 2017, Published online: 11 Oct 2017

References

  • Chan SL , AngX , SaniLLet al. Prevalence and characteristics of adverse drug reactions at admission to hospital: a prospective observational study . Br. J. Clin. Pharmacol.82 ( 6 ), 1636 – 1646 ( 2016 ).
  • International drug monitoring: the role of national centres . Report of a WHO meeting . WHO Tech. Rep. Ser.498 , 1 – 25 ( 1972 ).
  • Lazarou J , PomeranzBH , CoreyPN . Incidence of adverse drug reactions in hospitalized patients: a meta-analysis of prospective studies . JAMA279 ( 15 ), 1200 – 1205 ( 1998 ).
  • The European Commission document “Strengthening pharmacovigilance to reduce adverse effects of medicines ( 2008 ). http://europa.eu/rapid/press-release_MEMO-08-782_en.htm?locale=en .
  • Ernst FR , GrizzleAJ . Drug-related morbidity and mortality: updating the cost-of-illness model . J. Am. Pharm. Assoc. (Wash.)41 ( 2 ), 192 – 199 ( 2001 ).
  • Wysowski DK , SwartzL . Adverse drug event surveillance and drug withdrawals in the United States, 1969–2002: the importance of reporting suspected reactions . Arch. Intern. Med.165 ( 12 ), 1363 – 1369 ( 2005 ).
  • Rawlins MD , ThompsonJW . Pathogenesis of adverse drug reactions . In : Textbook of Adverse Drug Reactions . Oxford University Press , Oxford, UK ( 1977 ).
  • Pichler WJ , HausmannO . Classification of drug hypersensitivity into allergic, p-i, and pseudo-allergic forms . Int. Arch. Allergy Immunol.171 ( 3–4 ), 166 – 179 ( 2016 ).
  • Johansson SG , BieberT , DahlRet al. Revised nomenclature for allergy for global use: report of The Nomenclature Review Committee of the World Allergy Organization, October 2003 . J. Allergy Clin. Immunol.113 ( 5 ), 832 – 836 ( 2004 ).
  • Barbarino JM , KroetzDL , KleinTE , AltmanRB . PharmGKB summary: very important pharmacogene information for human leukocyte antigen B . Pharmacogenet. Genomics25 ( 4 ), 205 – 221 ( 2015 ).
  • Choo SY . The HLA system: genetics, immunology, clinical testing, and clinical implications . Yonsei Med. J.48 ( 1 ), 11 – 23 ( 2007 ).
  • Blackwell JM , JamiesonSE , BurgnerD . HLA and infectious diseases . Clin. Microbiol. Rev.22 ( 2 ), 370 – 385 ( 2009 ).
  • Gough SC , SimmondsMJ . The HLA region and autoimmune disease: associations and mechanisms of action . Curr. Genomics8 ( 7 ), 453 – 465 ( 2007 ).
  • Illing PT , MifsudNA , PurcellAW . Allotype specific interactions of drugs and HLA molecules in hypersensitivity reactions . Curr. Opin. Immunol.42 , 31 – 40 ( 2016 ).
  • Pichler WJ , AdamJ , DaubnerB , GentinettaT , KellerM , YerlyD . Drug hypersensitivity reactions: pathomechanism and clinical symptoms . Med. Clin. North Am.94 ( 4 ), 645 – 664 ( 2010 ).
  • Schnyder B , Mauri-HellwegD , ZanniM , BettensF , PichlerWJ . Direct, MHC-dependent presentation of the drug sulfamethoxazole to human alphabeta T-cell clones . J. Clin. Invest.100 ( 1 ), 136 – 141 ( 1997 ).
  • Naisbitt DJ , FarrellJ , WongGet al. Characterization of drug-specific T cells in lamotrigine hypersensitivity . J. Allergy Clin. Immunol.111 ( 6 ), 1393 – 1403 ( 2003 ).
  • Zanni MP , Von GreyerzS , SchnyderBet al. HLA-restricted, processing- and metabolism-independent pathway of drug recognition by human alpha beta T lymphocytes . J. Clin. Invest.102 ( 8 ), 1591 – 1598 ( 1998 ).
  • Pavlos R , MallalS , OstrovD , PompeuY , PhillipsE . Fever, rash, and systemic symptoms: understanding the role of virus and HLA in severe cutaneous drug allergy . J. Allergy Clin. Immunol. Pract.2 ( 1 ), 21 – 33 ( 2014 ).
  • Hetherington S , McguirkS , PowellGet al. Hypersensitivity reactions during therapy with the nucleoside reverse transcriptase inhibitor abacavir . Clin. Ther.23 ( 10 ), 1603 – 1614 ( 2001 ).
  • Chaponda M , PirmohamedM . Hypersensitivity reactions to HIV therapy . Br. J. Clin. Pharmacol.71 ( 5 ), 659 – 671 ( 2011 ).
  • Hetherington S , HughesAR , MostellerMet al. Genetic variations in HLA-B region and hypersensitivity reactions to abacavir . Lancet359 ( 9312 ), 1121 – 1122 ( 2002 ).
  • Mallal S , NolanD , WittCet al. Association between presence of HLA-B in situ 5701, HLA-DR7, and HLA-DQ3 and hypersensitivity to HIV-1 reverse-transcriptase inhibitor abacavir . Lancet359 ( 9308 ), 727 – 732 ( 2002 ).
  • Hughes DA , VilarFJ , WardCC , AlfirevicA , ParkBK , PirmohamedM . Cost–effectiveness analysis of HLA B in situ 5701 genotyping in preventing abacavir hypersensitivity . Pharmacogenetics14 ( 6 ), 335 – 342 ( 2004 ).
  • Rauch A , NolanD , MartinA , MckinnonE , AlmeidaC , MallalS . Prospective genetic screening decreases the incidence of abacavir hypersensitivity reactions in the Western Australian HIV cohort study . Clin. Infect. Dis.43 ( 1 ), 99 – 102 ( 2006 ).
  • Waters LJ , MandaliaS , GazzardB , NelsonM . Prospective HLA-B in situ 5701 screening and abacavir hypersensitivity: a single centre experience . AIDS21 ( 18 ), 2533 – 2534 ( 2007 ).
  • Zucman D , TruchisP , MajerholcC , StegmanS , Caillat-ZucmanS . Prospective screening for human leukocyte antigen-B in situ 5701 avoids abacavir hypersensitivity reaction in the ethnically mixed French HIV population . J. Acquir. Immune Defic. Syndr.45 ( 1 ), 1 – 3 ( 2007 ).
  • Mallal S , PhillipsE , CarosiGet al. HLA-B in situ 5701 screening for hypersensitivity to abacavir . N. Engl. J. Med.358 ( 6 ), 568 – 579 ( 2008 ).
  • Saag M , BaluR , PhillipsEet al. High sensitivity of human leukocyte antigen-b in situ 5701 as a marker for immunologically confirmed abacavir hypersensitivity in white and black patients . Clin. Infect. Dis.46 ( 7 ), 1111 – 1118 ( 2008 ).
  • Sousa-Pinto B , Pinto-RamosJ , CorreiaCet al. Pharmacogenetics of abacavir hypersensitivity: a systematic review and meta-analysis of the association with HLA-B in situ 57:01 . J. Allergy Clin. Immunol.136 ( 4 ), 1092 – 1094.e3 ( 2015 ).
  • EMA . European Medicines Agency . www.ema.europa.eu .
  • FDA . US Food and Drug Administration . www.fda.gov .
  • Zucman D , TruchisP , MajerholcC , StegmanS , Caillat-ZucmanS . Prospective screening for human leukocyte antigen-B in situ 5701 avoids abacavir hypersensitivity reaction in the ethnically mixed French HIV population . J. Acquir. Immune Defic. Syndr.45 ( 1 ), 1 – 3 ( 2007 ).
  • Small CB , MargolisDA , ShaeferMS , RossLL . HLA-B in situ 57:01 allele prevalence in HIV-infected North American subjects and the impact of allele testing on the incidence of abacavir-associated hypersensitivity reaction in HLA-B in situ 57:01 negative subjects . BMC Infect. Dis.17 ( 1 ), 256 ( 2017 ).
  • Ruiz-Iruela C , Padulles-ZamoraN , Podzamczer-PalterDet al. HLA-B in situ 57:01 genotyping in the prevention of hypersensitivity to abacavir: 5 years of experience . Pharmacogenet. Genomics26 ( 8 ), 390 – 396 ( 2016 ).
  • Nieves Calatrava D , Calle-Martin OdeL , Iribarren-LoyarteJAet al. Cost–effectiveness analysis of HLA-B in situ 5701 typing in the prevention of hypersensitivity to abacavir in HIV+ patients in Spain . Enferm. Infecc. Microbiol. Clin.28 ( 9 ), 590 – 595 ( 2010 ).
  • Chessman D , KostenkoL , LethborgTet al. Human leukocyte antigen class I-restricted activation of CD8+ T cells provides the immunogenetic basis of a systemic drug hypersensitivity . Immunity28 ( 6 ), 822 – 832 ( 2008 ).
  • Petros Z , KishikawaJ , MakonnenE , YimerG , HabtewoldA , AklilluE . HLA-B* 57 allele is associated with concomitant anti-tuberculosis and antiretroviral drugs induced liver toxicity in Ethiopians . Front. Pharmacol.8 , 90 ( 2017 ).
  • Xu CF , JohnsonT , WangXet al. HLA-B in situ 57:01 confers susceptibility to pazopanib-associated liver injury in patients with cancer . Clin. Cancer Res.22 ( 6 ), 1371 – 1377 ( 2016 ).
  • Daly AK , DonaldsonPT , BhatnagarPet al. HLA-B in situ 5701 genotype is a major determinant of drug-induced liver injury due to flucloxacillin . Nat. Genet.41 ( 7 ), 816 – 819 ( 2009 ).
  • Mockenhaupt M . The current understanding of Stevens–Johnson syndrome and toxic epidermal necrolysis . Expert Rev. Clin. Immunol.7 ( 6 ), 803 – 813 ( 2011 ).
  • Harr T , FrenchLE . Toxic epidermal necrolysis and Stevens–Johnson syndrome . Orphanet J. Rare Dis.5 , 39 ( 2010 ).
  • Kang HR , JeeYK , KimYSet al. Positive and negative associations of HLA class I alleles with allopurinol-induced SCARs in Koreans . Pharmacogenet. Genomics21 ( 5 ), 303 – 307 ( 2011 ).
  • Sousa-Pinto B , CorreiaC , GomesLet al. HLA and delayed drug-induced hypersensitivity . Int. Arch. Allergy Immunol.170 ( 3 ), 163 – 179 ( 2016 ).
  • Hershfield MS , CallaghanJT , TassaneeyakulWet al. Clinical Pharmacogenetics Implementation Consortium guidelines for human leukocyte antigen-B genotype and allopurinol dosing . Clin. Pharmacol. Ther.93 ( 2 ), 153 – 158 ( 2013 ).
  • Lee MT , MahasirimongkolS , ZhangYet al. Clinical application of pharmacogenomics: the example of HLA-based drug-induced toxicity . Public Health Genomics17 ( 5–6 ), 248 – 255 ( 2014 ).
  • Cheng CY , SuSC , ChenCH , ChenWL , DengST , ChungWH . HLA associations and clinical implications in T-cell mediated drug hypersensitivity reactions: an updated review . J. Immunol. Res.2014 , 565320 ( 2014 ).
  • Hung SI , ChungWH , LiouLBet al. HLA-B in situ 5801 allele as a genetic marker for severe cutaneous adverse reactions caused by allopurinol . Proc. Natl. Acad. Sci. USA102 ( 11 ), 4134 – 4139 ( 2005 ).
  • Tohkin M , KaniwaN , SaitoYet al. A whole-genome association study of major determinants for allopurinol-related Stevens–Johnson syndrome and toxic epidermal necrolysis in Japanese patients . Pharmacogenomics J.13 ( 1 ), 60 – 69 ( 2013 ).
  • Tassaneeyakul W , JantararoungtongT , ChenPet al. Strong association between HLA-B in situ 5801 and allopurinol-induced Stevens–Johnson syndrome and toxic epidermal necrolysis in a Thai population . Pharmacogenet. Genomics19 ( 9 ), 704 – 709 ( 2009 ).
  • Cao ZH , WeiZY , ZhuQYet al. HLA-B in situ 58:01 allele is associated with augmented risk for both mild and severe cutaneous adverse reactions induced by allopurinol in Han Chinese . Pharmacogenomics13 ( 10 ), 1193 – 1201 ( 2012 ).
  • Kaniwa N , SaitoY , AiharaMet al. HLA-B locus in Japanese patients with anti-epileptics and allopurinol-related Stevens–Johnson syndrome and toxic epidermal necrolysis . Pharmacogenomics9 ( 11 ), 1617 – 1622 ( 2008 ).
  • Lonjou C , BorotN , SekulaPet al. A European study of HLA-B in Stevens–Johnson syndrome and toxic epidermal necrolysis related to five high-risk drugs . Pharmacogenet. Genomics18 ( 2 ), 99 – 107 ( 2008 ).
  • Somkrua R , EickmanEE , SaokaewS , LohitnavyM , ChaiyakunaprukN . Association of HLA-B in situ 5801 allele and allopurinol-induced Stevens–Johnson syndrome and toxic epidermal necrolysis: a systematic review and meta-analysis . BMC Med. Genet.12 , 118 ( 2011 ).
  • Yun J , MattssonJ , SchnyderKet al. Allopurinol hypersensitivity is primarily mediated by dose-dependent oxypurinol-specific T-cell response . Clin. Exp. Allergy43 ( 11 ), 1246 – 1255 ( 2013 ).
  • Khanna D , FitzgeraldJD , KhannaPPet al. 2012 American College of Rheumatology guidelines for management of gout. Part 1: systematic nonpharmacologic and pharmacologic therapeutic approaches to hyperuricemia . Arthritis Care Res. (Hoboken)64 ( 10 ), 1431 – 1446 ( 2012 ).
  • Phillips EJ , MallalSA . Pharmacogenetics of drug hypersensitivity . Pharmacogenomics11 ( 7 ), 973 – 987 ( 2010 ).
  • Chung WH , HungSI , HongHSet al. Medical genetics: a marker for Stevens–Johnson syndrome . Nature428 ( 6982 ), 486 ( 2004 ).
  • Chung WH , HungSI . Recent advances in the genetics and immunology of Stevens–Johnson syndrome and toxic epidermal necrosis . J. Dermatol. Sci.66 ( 3 ), 190 – 196 ( 2012 ).
  • Man CB , KwanP , BaumLet al. Association between HLA-B in situ 1502 allele and antiepileptic drug-induced cutaneous reactions in Han Chinese . Epilepsia48 ( 5 ), 1015 – 1018 ( 2007 ).
  • Wu XT , HuFY , AnDMet al. Association between carbamazepine-induced cutaneous adverse drug reactions and the HLA-B in situ 1502 allele among patients in central China . Epilepsy Behav.19 ( 3 ), 405 – 408 ( 2010 ).
  • Wang Q , ZhouJQ , ZhouLMet al. Association between HLA-B in situ 1502 allele and carbamazepine-induced severe cutaneous adverse reactions in Han people of southern China mainland . Seizure20 ( 6 ), 446 – 448 ( 2011 ).
  • Tassaneeyakul W , TiamkaoS , JantararoungtongTet al. Association between HLA-B in situ 1502 and carbamazepine-induced severe cutaneous adverse drug reactions in a Thai population . Epilepsia51 ( 5 ), 926 – 930 ( 2010 ).
  • Locharernkul C , LoplumlertJ , LimotaiCet al. Carbamazepine and phenytoin induced Stevens–Johnson syndrome is associated with HLA-B in situ 1502 allele in Thai population . Epilepsia49 ( 12 ), 2087 – 2091 ( 2008 ).
  • Then SM , RaniZZ , RaymondAA , RatnaningrumS , JamalR . Frequency of the HLA-B in situ 1502 allele contributing to carbamazepine-induced hypersensitivity reactions in a cohort of Malaysian epilepsy patients . Asian Pac. J. Allergy Immunol.29 ( 3 ), 290 – 293 ( 2011 ).
  • Mehta TY , PrajapatiLM , MittalBet al. Association of HLA-B in situ 1502 allele and carbamazepine-induced Stevens–Johnson syndrome among Indians . Indian J. Dermatol. Venereol. Leprol.75 ( 6 ), 579 – 582 ( 2009 ).
  • Kulkantrakorn K , TassaneeyakulW , TiamkaoSet al. HLA-B in situ 1502 strongly predicts carbamazepine-induced Stevens–Johnson syndrome and toxic epidermal necrolysis in Thai patients with neuropathic pain . Pain Pract.12 ( 3 ), 202 – 208 ( 2012 ).
  • Grover S , KukretiR . HLA alleles and hypersensitivity to carbamazepine: an updated systematic review with meta-analysis . Pharmacogenet. Genomics24 ( 2 ), 94 – 112 ( 2014 ).
  • Tangamornsuksan W , ChaiyakunaprukN , SomkruaR , LohitnavyM , TassaneeyakulW . Relationship between the HLA-B in situ 1502 allele and carbamazepine-induced Stevens–Johnson syndrome and toxic epidermal necrolysis: a systematic review and meta-analysis . JAMA Dermatol.149 ( 9 ), 1025 – 1032 ( 2013 ).
  • Bloch KM , SillsGJ , PirmohamedM , AlfirevicA . Pharmacogenetics of antiepileptic drug-induced hypersensitivity . Pharmacogenomics15 ( 6 ), 857 – 868 ( 2014 ).
  • Chen P , LinJJ , LuCSet al. Carbamazepine-induced toxic effects and HLA-B in situ 1502 screening in Taiwan . N. Engl. J. Med.364 ( 12 ), 1126 – 1133 ( 2011 ).
  • Ko TM , ChungWH , WeiCYet al. Shared and restricted T-cell receptor use is crucial for carbamazepine-induced Stevens–Johnson syndrome . J. Allergy Clin. Immunol.128 ( 6 ), 1266 – 1276 ( 2011 ).
  • Ozeki T , MushirodaT , YowangAet al. Genome-wide association study identifies HLA-A in situ 3101 allele as a genetic risk factor for carbamazepine-induced cutaneous adverse drug reactions in Japanese population . Hum. Mol. Genet.20 ( 5 ), 1034 – 1041 ( 2011 ).
  • Mccormack M , AlfirevicA , BourgeoisSet al. HLA-A in situ 3101 and carbamazepine-induced hypersensitivity reactions in Europeans . N. Engl. J. Med.364 ( 12 ), 1134 – 1143 ( 2011 ).
  • Alfirevic A , JorgensenAL , WilliamsonPR , ChadwickDW , ParkBK , PirmohamedM . HLA-B locus in Caucasian patients with carbamazepine hypersensitivity . Pharmacogenomics7 ( 6 ), 813 – 818 ( 2006 ).
  • Niihara H , KakamuT , FujitaY , KanekoS , MoritaE . HLA-A31 strongly associates with carbamazepine-induced adverse drug reactions but not with carbamazepine-induced lymphocyte proliferation in a Japanese population . J. Dermatol.39 ( 7 ), 594 – 601 ( 2012 ).
  • Hung SI , ChungWH , JeeSHet al. Genetic susceptibility to carbamazepine-induced cutaneous adverse drug reactions . Pharmacogenet. Genomics16 ( 4 ), 297 – 306 ( 2006 ).
  • Wei CY , ChungWH , HuangHW , ChenYT , HungSI . Direct interaction between HLA-B and carbamazepine activates T cells in patients with Stevens–Johnson syndrome . J. Allergy Clin. Immunol.129 ( 6 ), 1562 – 1569 ( 2012 ).
  • Sukasem C , PuangpetchA , MedhasiS , TassaneeyakulW . Pharmacogenomics of drug-induced hypersensitivity reactions: challenges, opportunities and clinical implementation . Asian Pac. J. Allergy Immunol.32 ( 2 ), 111 – 123 ( 2014 ).
  • Amstutz U , ShearNH , RiederMJet al. Recommendations for HLA-B in situ 15:02 and HLA-A in situ 31:01 genetic testing to reduce the risk of carbamazepine-induced hypersensitivity reactions . Epilepsia55 ( 4 ), 496 – 506 ( 2014 ).
  • Yip VL , PirmohamedM . The HLA-A in situ 31:01 allele: influence on carbamazepine treatment . Pharmgenomics Pers. Med.10 , 29 – 38 ( 2017 ).
  • Hung SI , ChungWH , LiuZSet al. Common risk allele in aromatic antiepileptic-drug induced Stevens–Johnson syndrome and toxic epidermal necrolysis in Han Chinese . Pharmacogenomics11 ( 3 ), 349 – 356 ( 2010 ).
  • Liao WP , ShiYW , MinFL . HLA-B in situ 1502 screening and toxic effects of carbamazepine . N. Engl. J. Med.365 ( 7 ), 672 – 673 ( 2011 ).
  • Plumpton CO , RobertsD , PirmohamedM , HughesDA . A systematic review of economic evaluations of pharmacogenetic testing for prevention of adverse drug reactions . Pharmacoeconomics34 ( 8 ), 771 – 793 ( 2016 ).
  • Whirl-Carrillo M , McdonaghEM , HebertJMet al. Pharmacogenomics knowledge for personalized medicine . Clin. Pharmacol. Ther.92 ( 4 ), 414 – 417 ( 2012 ).
  • PharmGBK . www.pharmgkb.org/ .
  • Pirmohamed M . Acceptance of biomarker-based tests for application in clinical practice: criteria and obstacles . Clin. Pharmacol. Ther.88 ( 6 ), 862 – 866 ( 2010 ).
  • Alfirevic A , PirmohamedM . Genomics of adverse drug reactions . Trends Pharmacol. Sci.38 ( 1 ), 100 – 109 ( 2017 ).
  • Lauschke VM , Ingelman-SundbergM . Requirements for comprehensive pharmacogenetic genotyping platforms . Pharmacogenomics17 ( 8 ), 917 – 924 ( 2016 ).
  • St Sauver JL , BielinskiSJ , OlsonJEet al. Integrating pharmacogenomics into clinical practice: promise vs reality . Am. J. Med.129 ( 10 ), 1093 – 1099 ( 2016 ).
  • Yun J , AdamJ , YerlyD , PichlerWJ . Human leukocyte antigens (HLA) associated drug hypersensitivity: consequences of drug binding to HLA . Allergy67 ( 11 ), 1338 – 1346 ( 2012 ).
  • Bharadwaj M , IllingP , KostenkoL . Personalized medicine for HLA-associated drug-hypersensitivity reactions . Personalized Med.7 ( 5 ), 495 – 516 ( 2010 ).
  • Karlin E , PhillipsE . Genotyping for severe drug hypersensitivity . Curr. Allergy Asthma Rep.14 ( 3 ), 418 ( 2014 ).
  • Alfirevic A , PirmohamedM . Predictive genetic testing for drug-induced liver injury: considerations of clinical utility . Clin. Pharmacol. Ther.92 ( 3 ), 376 – 380 ( 2012 ).
  • Bjornsson ES , BergmannOM , BjornssonHK , KvaranRB , OlafssonS . Incidence, presentation, and outcomes in patients with drug-induced liver injury in the general population of Iceland . Gastroenterology144 ( 7 ), 1419 – 1425 ( 2013 ).
  • Becquemont L . HLA: a pharmacogenomics success story . Pharmacogenomics11 ( 3 ), 277 – 281 ( 2010 ).
  • Sharon E , StreicherH , GoncalvesP , ChenHX . Immune checkpoint inhibitors in clinical trials . Chinese J. Cancer33 ( 9 ), 434 – 444 ( 2014 ).
  • Roberts K , CulletonV , LwinZ , O’ByrneK , HughesBG . Immune checkpoint inhibitors: navigating a new paradigm of treatment toxicities . Asia Pac. J. Clin. Oncol.13 ( 4 ), 277 – 288 ( 2017 ).
  • Ciccarese C , AlfieriS , SantoniMet al. New toxicity profile for novel immunotherapy agents: focus on immune-checkpoint inhibitors . Expert Opin. Drug Metab. Toxicol.12 ( 1 ), 57 – 75 ( 2016 ).
  • Demlova R , ValikD , ObermannovaR , Zdrazilova-DubskaL . The safety of therapeutic monoclonal antibodies: implications for cancer therapy including immuno-checkpoint inhibitors . Physiol. Res.65 ( Suppl. 4 ), S455 – S462 ( 2016 ).

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