Genetics of Immune-Mediated Adverse Drug Reactions: a Comprehensive and Clinical Review

Clinical Reviews in Allergy and Immunology

Volumn 48, Issue 2-3, 2015, Pages 165-175

  Yip, V L M ^a   Alfirevic, A ^a   Pirmohamed, M ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Abacavir; Adverse drug reactions; Allopurinol; Carbamazepine; Drug induced liver injury; Drug induced skin injury; Flucloxacillin; Human leukocyte antigen; Hypersensitivity; Hypersensitivity syndrome; Maculopapular exanthema; Stevens Johnson syndrome; Ximelagatran

Indexed keywords

CHEMICALLY INDUCED; DRUG HYPERSENSITIVITY; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; GENETIC PREDISPOSITION; GENETICS; HUMAN; IMMUNOLOGY; PHENOTYPE; SKIN DISEASE; TOXIC HEPATITIS;

DRUG HYPERSENSITIVITY; DRUG-INDUCED LIVER INJURY; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; PHENOTYPE; SKIN DISEASES;

EID: 84939894832     PISSN: 10800549     EISSN: 15590267     Source Type: Journal    
DOI: 10.1007/s12016-014-8418-y     Document Type: Review

References (111)

1. Aronson JK, Ferner RE (2005) Clarification of terminology in drug safety. Drug Saf 28(10):851–870
2. Pirmohamed M, James S, Meakin S et al (2004) Adverse drug reactions as cause of admission to hospital: prospective analysis of 18,820 patients. BMJ: Br Med J 7456:15–19
3. Davies EC, Mottram DR, Green CF, Taylor S, Williamson PR, Pirmohamed M (2009) Adverse drug reactions in hospital in-patients: a prospective analysis of 3695 patient-episodes. PLoS ONE 4(2):e4439
4. Lazarou J, Pomeranz BH, Corey PN (1998) Incidence of adverse drug reactions in hospitalized patients: a meta-analysis of prospective studies. JAMA J Am Med Assoc 279(15):1200–1205
5. FDA Centre for Drug Evaluation and Research (2005) Report to the Nation 2005: Improving Public Health through Drugs. http://www.fda.gov/downloads/AboutFDA/CentersOffices/CDER/WhatWeDo/UCM078935.pdf. Accessed 14 Jan 2013
6. Rawlins M, Thompson J (1991) Mechanisms of adverse drug reactions. In Textbook of Adverse Drug Reactions. Oxford University Press, Oxford
7. Pirmohamed M (2012) Genetics and the potential for predictive tests in adverse drug reactions. Chem Immunol Allergy 97:18–31
8. Mallal S, Nolan D, Witt C et al (2002) Association between presence of HLA-B*5701, HLA-DR7, and HLA-DQ3 and hypersensitivity to HIV-1 reverse-transcriptase inhibitor abacavir. Lancet 359(9308):727–732
9. Chung W-H, Hung S-I, Hong H-S et al (2004) Medical genetics: a marker for Stevens-Johnson syndrome. Nature 428(6982):486–486
10. McCormack M, Alfirevic A, Bourgeois S et al (2011) HLA-A*3101 and carbamazepine-induced hypersensitivity reactions in Europeans. N Engl J Med 364(12):1134–1143
11. Hautekeete ML, Horsmans Y, Van Waeyenberge C et al (1999) HLA association of amoxicillin-clavulanate-induced hepatitis. Gastroenterology 117(5):1181–1186
12. Becquemont L (2010) HLA: a pharmacogenomics success story. Pharmacogenomics 11(3):277–281
13. Pirmohamed M, Aithal GP, Behr E, Daly A, Roden D (2011) The phenotype standardization project: improving pharmacogenetic studies of serious adverse drug reactions. Clin Pharmacol Ther 89(6):784–785
14. Pirmohamed M, Friedmann PS, Molokhia M et al (2011) Phenotype standardization for immune-mediated drug-induced skin injury. Clin Pharmacol Ther 89(6):896–901
15. Aithal GP, Watkins PB, Andrade RJ et al (2011) Case definition and phenotype standardization in drug-induced liver injury. Clin Pharmacol Ther 89(6):806–815
16. Pirmohamed M, Park BK (2001) Genetic susceptibility to adverse drug reactions. Trends Pharmacol Sci 22(6):298–305
17. Alfirevic A, Pirmohamed M (2010) Drug-induced hypersensitivity reactions and pharmacogenomics: past, present and future. Pharmacogenomics 11(4):497–499
18. Roujeau J-C, Kelly JP, Naldi L et al (1995) Medication use and the risk of Stevens–Johnson syndrome or toxic epidermal necrolysis. N Engl J Med 333(24):1600–1608
19. Hetherington S, Hughes AR, Mosteller M et al (2002) Genetic variations in HLA-B region and hypersensitivity reactions to abacavir. Lancet 359(9312):1121–1122
20. Hughes D, Vilar F, Ward C, Alfirevic A, Park BK, Pirmohamed M (2004) Cost-effectiveness analysis of HLA B*5701 genotyping in preventing abacavir hypersensitivity. Pharmacogenetics 14:335–342
21. Mallal S, Phillips E, Nolan D et al (2008) HLA-B*5701 screening for hypersensitivity to abacavir. N Engl J Med 358(6):568–579
22. Saag M, Balu R, Phillips E et al (2008) High sensitivity of human leukocyte antigen-B*5701 as a marker for immunologically confirmed abacavir hypersensitivity in white and black patients. Clin Infect Dis 46(7):1111–1118
23. Man CBL, Kwan P, Baum L et al (2007) Association between HLA-B*1502 allele and antiepileptic drug-induced cutaneous reactions in Han Chinese. Epilepsia 48(5):1015–1018
24. Wu XT, Hu FY, An DM et al (2010) Association between carbamazepine-induced cutaneous adverse drug reactions and the HLA-B*1502 allele among patients in central China. Epilepsy Behav 19(3):405–408
25. Wang Q, Zhou J-Q, Zhou L-M et al (2011) Association between HLA-B*1502 allele and carbamazepine-induced severe cutaneous adverse reactions in Han people of southern China mainland. Seizure 20(6):446–448
26. Hung S-I, Chung W-H, Jee S-H et al (2006) Genetic susceptibility to carbamazepine-induced cutaneous adverse drug reactions. Pharmacogenet Genomics 16(4):297–306
27. Tassaneeyakul W, Tiamkao S, Jantararoungtong T et al (2010) Association between HLA-B*1502 and carbamazepine-induced severe cutaneous adverse drug reactions in a Thai population. Epilepsia 51(5):926–930
28. Locharernkul C, Loplumlert J, Limotai C et al (2008) Carbamazepine and phenytoin induced Stevens-Johnson syndrome is associated with HLA-B*1502 allele in Thai population. Epilepsia 49(12):2087–2091
29. Then SM, Rani ZZM, Raymond AA, Ratnaningrum S, Jamal R (2011) Frequency of the HLA-B*1502 allele contributing to carbamazepine-induced hypersensitivity reactions in a cohort of Malaysian epilepsy patients. Asian Pac J Allergy Immunol 29(3):290–293
30. Mehta TY, Prajapati LM, Mittal B et al (2009) Association of HLA-B*1502 allele and carbamazepine-induced Stevens-Johnson syndrome among Indians. Indian J Dermatol Venereol Leprol 75(6):579–582
31. Ozeki T, Mushiroda T, Yowang A et al (2011) 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 20(5):1034–1041
32. Kim S-H, Lee KW, Song W-J et al (2011) Carbamazepine-induced severe cutaneous adverse reactions and HLA genotypes in Koreans. Epilepsy Res 97(1–2):190–197
33. Hung S-I, Chung W-H, Liou L-B et al (2005) HLA-B*5801 allele as a genetic marker for severe cutaneous adverse reactions caused by allopurinol. Proc Natl Acad Sci USA 102(11):4134–4139
34. Tassaneeyakul W, Jantararoungtong T, Vannaprasaht S et al (2009) Strong association between HLA-B*5801 and allopurinol-induced Stevens-Johnson syndrome and toxic epidermal necrolysis in a Thai population. Pharmacogenet Genomics 19(9):704–709
35. Kaniwa N, Saito Y, Aihara M et al (2008) HLA-B locus in Japanese patients with anti-epileptics and allopurinol-related Stevens–Johnson syndrome and toxic epidermal necrolysis. Pharmacogenomics 9(11):1617–1622
36. Ding WY, Lee CK, Choon SE et al (2010) Cutaneous adverse drug reactions seen in a tertiary hospital in Johor, Malaysia. Int J Dermatol 49(7):834
37. Kazeem GR, Cox C, Aponte J et al (2009) High-resolution HLA genotyping and severe cutaneous adverse reactions in lamotrigine-treated patients. Pharmacogenet Genomics 19(9):661
38. Martin AM, Nolan D, James I et al (2005) Predisposition to nevirapine hypersensitivity associated with HLA-DRB1 0101 and abrogated by low CD4 T-cell counts. AIDS 19(1):97
39. Vitezica ZG, Milpied B, Lonjou C et al (2008) HLA-DRB1 01 associated with cutaneous hypersensitivity induced by nevirapine and efavirenz. AIDS 22(4):540
40. Littera R, Carcassi C, Masala A et al (2006) HLA-dependent hypersensitivity to nevirapine in Sardinian HIV patients. AIDS 20(12):1621
41. Gatanaga H, Yazaki H, Tanuma J et al (2007) HLA-Cw8 primarily associated with hypersensitivity to nevirapine. AIDS 21(2):264
42. Chantarangsu S, Mushiroda T, Mahasirimongkol S et al (2009) HLA-B 3505 allele is a strong predictor for nevirapine-induced skin adverse drug reactions in HIV-infected Thai patients. Pharmacogenet Genomics 19(2):139
43. Umapathy S, Pawar A, Bajpai S, Pazare AR, Ghosh K (2011) HLA involvement in nevirapine-induced dermatological reaction in antiretroviral-treated HIV-1 patients. J Pharmacol Pharmacother 2(2):114–115
44. Likanonsakul S, Rattanatham T, Feangvad S et al (2009) HLA-Cw*04 allele associated with nevirapine-induced rash in HIV-infected Thai patients. AIDS Res Ther 6:22
45. Gao S, Gui X-E, Liang K et al (2012) HLA-dependent hypersensitivity reaction to nevirapine in Chinese Han HIV-infected patients. AIDS Res Hum Retrovir 28(6):540
46. Lonjou C, Borot N, Ledger N et al (2008) A European study of HLA-B in Stevens-Johnson syndrome and toxic epidermal necrolysis related to five high-risk drugs. Pharmacogenet Genomics 18(2):99–107
47. Roujeau J-C, Bracq C, Huyn NT, Chaussalet E, Raffin C, Duédari N (1986) HLA phenotypes and bullous cutaneous reactions to drugs. Tissue Antigens 28(4):251–254
48. Romano A, Fonso MD, Venuti A et al (1998) Delayed hypersensitivity to aminopenicillins is related to major histocompatibility complex genes. Ann Allergy Asthma Immunol 80(5):433–437
49. Özkaya-Bayazit E, Akar U (2001) Fixed drug eruption induced by trimethoprim-sulfamethoxazole: evidence for a link to HLA-A30 B13 Cw6 haplotype. J Am Acad Dermatol 45(5):712–717
50. Hetherington S, McGuirk S, Powell G et al (2001) Hypersensitivity reactions during therapy with the nucleoside reverse transcriptase inhibitor abacavir. Clin Ther 23(10):1603–1614
51. Phillips EJ, Sullivan JR, Knowles SR, Shear NH (2002) Utility of patch testing in patients with hypersensitivity syndromes associated with abacavir. AIDS 16(16):2223–2225
52. Symonds W, Cutrell A, Edwards M et al (2002) Risk factor analysis of hypersensitivity reactions to abacavir. Clin Ther 24(4):565–573
53. Peyrieère H et al (2001) Hypersensitivity related to abacavir in two members of a family. Ann Pharmacother 35(10):1291
54. Nolan D, Martin A, Almeida C, Mallal S (2006) Prospective genetic screening decreases the incidence of abacavir hypersensitivity reactions in the Western Australian HIV cohort study. Clin Infect Dis 43(1):99–102
55. Waters LJ, Mandalia S, Gazzard B, Nelson M (2007) Prospective HLA-B*5701 screening and abacavir hypersensitivity: a single centre experience. AIDS 21(18):2533–2534
56. Zucman D, Majerholc C, Truchis PD, Stegman S, Caillat-Zucman S (2007) Prospective screening for human leukocyte antigen-B*5701 avoids abacavir hypersensitivity reaction in the ethnically mixed French HIV population. J Acquir Immune Defic Syndr 45(1):1–3
57. Colombo S, Rotger M, Martinez R et al (2008) The HCP5 single-nucleotide polymorphism: a simple screening tool for prediction of hypersensitivity reaction to abacavir. J Infect Dis 198(6):864–867
58. Dello Russo C, Lisi L, Lofaro A et al (2011) Novel sensitive, specific and rapid pharmacogenomic test for the prediction of abacavir hypersensitivity reaction: HLA-B*57:01 detection by real-time PCR. Pharmacogenomics 12(4):567–576
59. Kauf TL, Farkouh RA, Earnshaw SR, Watson ME, Maroudas P, Chambers MG (2010) Economic efficiency of genetic screening to inform the use of abacavir sulfate in the treatment of HIV. PharmacoEconomics 28(11):1025–1039
60. Schackman BR, Scott CA, Walensky RP, Losina E, Freedberg KA, Sax PE (2008) The cost-effectiveness of HLA-B*5701 genetic screening to guide initial antiretroviral therapy for HIV. AIDS 22(15):2025–2033
61. Marson AG, Al-Kharusi AM, Alwaidh M et al (2007) The SANAD study of effectiveness of carbamazepine, gabapentin, lamotrigine, oxcarbazepine, or topiramate for treatment of partial epilepsy: an unblinded randomised controlled trial. Lancet 369(9566):1000–1015
62. Post RM, Ketter TA, Uhde T, Ballenger JC (2007) Thirty years of clinical experience with carbamazepine in the treatment of bipolar illness: principles and practice. CNS Drugs 21(1):47–71
63. Cruccu G, Gronseth G, Alksne J et al (2008) AAN-EFNS guidelines on trigeminal neuralgia management. Eur J Neurol Off J Eur Fed Neurol Soc 15(10):1013–1028
64. Wu Y, Farrell J, Pirmohamed M, Park BK, Naisbitt DJ (2007) Generation and characterization of antigen-specific CD4+, CD8+, and CD4 + CD8+ T-cell clones from patients with carbamazepine hypersensitivity. J Allergy Clin Immunol 119(4):973–981
65. Alfirevic A, Jorgensen AL, Williamson PR, Chadwick DW, Park BK, Pirmohamed M (2006) HLA-B locus in Caucasian patients with carbamazepine hypersensitivity. Pharmacogenomics 7(6):813–818
66. Lonjou C, Thomas L, Borot N et al (2006) A marker for Stevens-Johnson syndrome: ethnicity matters. Pharmacogenomics J 6(4):265–268
67. Kano Y, Hirahara K, Asano Y, Shiohara T (2008) HLA-B allele associations with certain drugs are not confirmed in Japanese patients with severe cutaneous drug reactions. Acta Derm Venereol 88(6):616–618
68. Lim KS, Tan CT, Kwan P (2008) Association of HLA-B*1502 allele and carbamazepine-induced severe adverse cutaneous drug reaction among Asians, a review. Neurol Asia 13:15–21
69. Yip VL, Marson AG, Jorgensen AL, Pirmohamed M, Alfirevic A (2012) HLA genotype and carbamazepine-induced cutaneous adverse drug reactions: a systematic review. Clin Pharmacol Ther 92(6):757–765
70. Chen P, Lin J-J, Lu C-S et al (2011) Carbamazepine-induced toxic effects and HLA-B*1502 screening in Taiwan. N Engl J Med 364(12):1126–1133
71. Locharernkul C, Shotelersuk V, Hirankarn N (2010) HLA-B* 1502 screening: time to clinical practice. Epilepsia 51(5):936–938
72. Ferrell PB, McLeod HL (2008) Carbamazepine, HLA-B*1502 and risk of Stevens–Johnson syndrome and toxic epidermal necrolysis: US FDA recommendations. Pharmacogenomics 9(10):1543–1546
73. Kang HR, Kim YS, Jung JW et al (2011) Positive and negative associations of HLA class i alleles with allopurinol-induced SCARs in Koreans. Pharmacogenet Genomics 21(5):303–307
74. Ostapowicz G, Fontana RJ, Schiødt FV et al (2002) Results of a prospective study of acute liver failure at 17 tertiary care centers in the United States. Ann Intern Med 137(12):947–954
75. Sgro C, Clinard F, Ouazir K et al (2002) Incidence of drug-induced hepatic injuries: a French population-based study. Hepatology 36(2):451–455
76. Björnsson E, Jerlstad P, Olsson R, Bergqvist A (2005) Fulminant drug-induced hepatic failure leading to death or liver transplantation in Sweden. Scand J Gastroenterol 40(9):1095–1101
77. Temple R (2006) Hepatotoxicity through the years. www.fda.gov/downloads/Drugs/ScienceResearch/ResearchAreas/ucm122149.pdf. Accessed 23 Jan 2013
78. Russmann S, Kullak-Ublick GA, Grattagliano I (2009) Current concepts of mechanisms in drug-induced hepatotoxicity. Curr Med Chem 16(23):3041–3053
79. O’Donohue J, Mills PR, Oien KA et al (2000) Co-amoxiclav jaundice: clinical and histological features and HLA class II association. Gut 47(5):717–720
80. Donaldson PT, Daly AK, Henderson J et al (2010) Human leucocyte antigen class II genotype in susceptibility and resistance to co-amoxiclav-induced liver injury. J Hepatol 53(6):1049–1053
81. Lucena MI, Andrade RJ, Stephens C et al (2011) Susceptibility to amoxicillin-clavulanate-induced liver injury is influenced by multiple HLA class i and II alleles. Gastroenterology 141(1):338–347
82. Daly AK, Donaldson PT, Bhatnagar P et al (2009) HLA-B*5701 genotype is a major determinant of drug-induced liver injury due to flucloxacillin. Nat Genet 41(7):816–819
83. Kindmark A, Jawaid A, Harbron CG et al (2008) Genome-wide pharmacogenetic investigation of a hepatic adverse event without clinical signs of immunopathology suggests an underlying immune pathogenesis. Pharmacogenomics J 8(3):186–195
84. Singer JB, Lewitzky S, Leroy E et al (2010) A genome-wide study identifies HLA alleles associated with lumiracoxib-related liver injury. Nat Genet 42(8):711–714
85. Yuan J, Guo S, Huang Z et al (2011) Toxicogenomics of nevirapine-associated cutaneous and hepatic adverse events among populations of African, Asian, and European descent. AIDS 25(10):1271–1280
86. Spraggs CF, Budde LR, Briley LP et al (2011) HLA-DQA1*02:01 is a major risk factor for lapatinib-induced hepatotoxicity in women with advanced breast cancer. J Clin Oncol 29(6):667–673
87. Hirata K, Yamamoto M, Okutani Y et al (2008) Ticlopidine-induced hepatotoxicity is associated with specific human leukocyte antigen genomic subtypes in Japanese patients: a preliminary case–control study. Pharmacogenomics J 8(1):29–33
88. Ariyoshi N, Iga Y, Hirata K et al (2010) Enhanced susceptibility of HLA-mediated ticlopidine-induced idiosyncratic hepatotoxicity by CYP2B6 polymorphism in Japanese. Drug Metab Pharmacokinet 25(3):298
89. Andrade RJ, García-Ruiz E, García-Muñoz B et al (2005) Drug-induced liver injury: an analysis of 461 incidences submitted to the Spanish registry over a 10-year period. Gastroenterology 129(2):512–521
90. Chalasani N, Fontana RJ, Bonkovsky HL et al (2008) Causes, clinical features, and outcomes from a prospective study of drug-induced liver injury in the United States. Gastroenterology 135(6):1924–1934, e1924
91. García Rodríguez LA, Stricker BH, Zimmerman HJ (1996) Risk of acute liver injury associated with the combination of amoxicillin and clavulanic acid. Arch Intern Med 156(12):1327–1332
92. Fontana RJ, Shakil AO, Greenson JK, Boyd I, Lee WM (2005) Acute liver failure due to amoxicillin and amoxicillin/clavulanate. Dig Dis Sci 50(10):1785–1790
93. Andrade RJ, Lucena MI, Alonso A et al (2004) HLA class II genotype influences the type of liver injury in drug-induced idiosyncratic liver disease. Hepatology (Baltimore, Md) 39(6):1603–1612
94. Russmann S, Kaye JA, Jick SS, Jick H (2005) Risk of cholestatic liver disease associated with flucloxacillin and flucloxacillin prescribing habits in the UK: cohort study using data from the UK General Practice Research Database. Br J Clin Pharmacol 60(1):76–82
95. Alfirevic A, Pirmohamed M (2012) Predictive genetic testing for drug-induced liver injury: considerations of clinical utility. Clin Pharmacol Ther 92(3):376–380
96. Testa L, Bhindi R, Van Gaal WJ, Agostoni P, Abbate A, Biondi Zoccai GGL (2007) The direct thrombin inhibitor ximelagatran/melagatran: a systematic review on clinical applications and an evidence based assessment of risk benefit profile. Expert Opin Drug Saf 6(4):397–406
97. Bonierbale E, Valadon P, Pons C et al (1999) Opposite behaviors of reactive metabolites of tienilic acid and its isomer toward liver proteins: use of specific anti-tienilic acid & minus; protein adduct antibodies and the possible relationship with different hepatotoxic effects of the two compounds. Chem Res Toxicol 12(3):286
98. Aithal GP, Rawlins MD, Day CP (1999) Accuracy of hepatic adverse drug reaction reporting in one English health region. BMJ (Clin Res Ed) 319(7224):1541
99. Rockey DC, Seeff LB, Rochon J et al (2010) Causality assessment in drug-induced liver injury using a structured expert opinion process: comparison to the Roussel-Uclaf causality assessment method. Hepatology 51(6):2117–2126
100. Chessman D, Kostenko L, Lethborg T et al (2008) Human leukocyte antigen class I-restricted activation of CD8+ T cells provides the immunogenetic basis of a systemic drug hypersensitivity. Immunity 28(6):822
101. Alfirevic A, Gonzalez-Galarza F, Bell C et al (2012) In silico analysis of HLA associations with drug-induced liver injury: use of a HLA-genotyped DNA archive from healthy volunteers. Genome Med 4(6):51
102. Evans WE (2004) Pharmacogenetics of thiopurine S-methyltransferase and thiopurine therapy. Ther Drug Monit 26(2):186–191
103. Lindh JD, Holm L, Andersson ML et al (2009) Influence of CYP2C9 genotype on warfarin dose requirements—a systematic review and meta-analysis. Eur J Clin Pharmacol 65(4):365
104. Innocenti F, Undevia SD, Iyer L et al (2004) Genetic variants in the UDP-glucuronosyltransferase 1A1 gene predict the risk of severe neutropenia of irinotecan. J Clin Oncol 22(8):1382–1388
105. Youngster I, Arcavi L, Schechmaster R et al (2010) Medications and glucose-6-phosphate dehydrogenase deficiency: an evidence-based review. Drug Saf 33(9):713
106. Brugts JJ, Isaacs A, Boersma E et al (2010) Genetic determinants of treatment benefit of the angiotensin-converting enzyme-inhibitor perindopril in patients with stable coronary artery disease. Eur Heart J 31(15):1854
107. Veenstra D, Higashi M, Phillips K, Veenstra DL, Higashi MK, Phillips KA (2000) Assessing the cost-effectiveness of pharmacogenomics. AAPS PharmSci 2(3):80
108. Bodmer W, Bonilla C, Bodmer W et al (2008) Common and rare variants in multifactorial susceptibility to common diseases. Nat Genet 40(6):695
109. Szyf M, Szyf M, Szyf M (2007) The dynamic epigenome and its implications in toxicology. Toxicol Sci 100(1):7
110. Kacevska M, Ivanov M, Ingelman-Sundberg M (2011) Perspectives on epigenetics and its relevance to adverse drug reactions. Clin Pharmacol Ther 89(6):902–907
111. Pirmohamed M (2010) Acceptance of biomarker-based tests for application in clinical practice: criteria and obstacles. Clin Pharmacol Ther 88(6):862–866