Association Between HLA-B*1301 and Dapsone-Induced Cutaneous Adverse Drug Reactions: A Systematic Review and Meta-analysis | Dermatology | JAMA Dermatology | JAMA Network
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Figure 1.  PRISMA Flow Diagram of HLA-B*1301 and Dapsone-Induced Cutaneous Adverse Drug Reactions (cADRs)
PRISMA Flow Diagram of HLA-B*1301 and Dapsone-Induced Cutaneous Adverse Drug Reactions (cADRs)

Summary of study identification, inclusion, and exclusion. HuGENet indicates Human Genome Epidemiology Network.

Figure 2.  Associations Between HLA-B*1301 and Dapsone-Induced Cutaneous Adverse Drug Reactions (cADRs)
Associations Between HLA-B*1301 and Dapsone-Induced Cutaneous Adverse Drug Reactions (cADRs)

Forest plot shows associations between HLA-B*1301 and dapsone-induced cADRs using dapsone-tolerant controls. Each data marker and its size indicate a mean value and a magnitude of the data point compared with the total. Error bars indicate 95% CIs and vertical dotted line, overall estimated odds ratio (OR). Data marker size reflects the weight of the study using random-effects meta-analysis. Data were evaluated using R, version 3.4.3 (The R Foundation).

Table 1.  Characteristics of the 3 Included Studies
Characteristics of the 3 Included Studies
Table 2.  Calculated ORs of the 3 Included Studies and Summary ORs Categorized by Type of Control and cADR
Calculated ORs of the 3 Included Studies and Summary ORs Categorized by Type of Control and cADR
1.
Zhu  YI, Stiller  MJ.  Dapsone and sulfones in dermatology: overview and update.  J Am Acad Dermatol. 2001;45(3):420-434.PubMedGoogle ScholarCrossref
2.
Kannan  G, Vasantha  J, Rani  NV,  et al.  Drug usage evaluation of dapsone.  Indian J Pharm Sci. 2009;71(4):456-460.PubMedGoogle ScholarCrossref
3.
Wozel  G, Blasum  C.  Dapsone in dermatology and beyond.  Arch Dermatol Res. 2014;306(2):103-124.PubMedGoogle ScholarCrossref
4.
Kosseifi  SG, Guha  B, Nassour  DN, Chi  DS, Krishnaswamy  G.  The dapsone hypersensitivity syndrome revisited: a potentially fatal multisystem disorder with prominent hepatopulmonary manifestations.  J Occup Med Toxicol. 2006;1:9.PubMedGoogle ScholarCrossref
5.
Vinod  KV, Arun  K, Dutta  TK.  Dapsone hypersensitivity syndrome: a rare life threatening complication of dapsone therapy.  J Pharmacol Pharmacother. 2013;4(2):158-160.PubMedGoogle ScholarCrossref
6.
Lorenz  M, Wozel  G, Schmitt  J.  Hypersensitivity reactions to dapsone: a systematic review.  Acta Derm Venereol. 2012;92(2):194-199.PubMedGoogle ScholarCrossref
7.
Tian  W, Shen  J, Zhou  M, Yan  L, Zhang  G.  Dapsone hypersensitivity syndrome among leprosy patients in China.  Lepr Rev. 2012;83(4):370-377.PubMedGoogle Scholar
8.
Pandey  B, Shrestha  K, Lewis  J, Hawksworth  RA, Walker  SL.  Mortality due to dapsone hypersensitivity syndrome complicating multi-drug therapy for leprosy in Nepal.  Trop Doct. 2007;37(3):162-163.PubMedGoogle ScholarCrossref
9.
Chung  WH, Hung  SI, Chen  YT.  Human leukocyte antigens and drug hypersensitivity.  Curr Opin Allergy Clin Immunol. 2007;7(4):317-323.PubMedGoogle ScholarCrossref
10.
Bharadwaj  M, Illing  P, Kostenko  L.  Personalized medicine for HLA-associated drug-hypersensitivity reactions.  Per Med. 2010;7(5):495-516. doi:10.2217/pme.10.46Google ScholarCrossref
11.
Somkrua  R, Eickman  EE, Saokaew  S, Lohitnavy  M, Chaiyakunapruk  N.  Association of HLA-B*5801 allele and allopurinol-induced Stevens Johnson syndrome and toxic epidermal necrolysis: a systematic review and meta-analysis.  BMC Med Genet. 2011;12:118.PubMedGoogle ScholarCrossref
12.
Tangamornsuksan  W, Lohitnavy  O, Kongkaew  C,  et al.  Association of HLA-B*5701 genotypes and abacavir-induced hypersensitivity reaction: a systematic review and meta-analysis.  J Pharm Pharm Sci. 2015;18(1):68-76.PubMedGoogle ScholarCrossref
13.
Tangamornsuksan  W, Chaiyakunapruk  N, Somkrua  R, Lohitnavy  M, Tassaneeyakul  W.  Relationship between the HLA-B*1502 allele and carbamazepine-induced Stevens-Johnson syndrome and toxic epidermal necrolysis: a systematic review and meta-analysis.  JAMA Dermatol. 2013;149(9):1025-1032.PubMedGoogle ScholarCrossref
14.
Chen  CB, Hsiao  YH, Wu  T,  et al; Taiwan Severe Cutaneous Adverse Reaction Consortium.  Risk and association of HLA with oxcarbazepine-induced cutaneous adverse reactions in Asians.  Neurology. 2017;88(1):78-86.PubMedGoogle ScholarCrossref
15.
Wang  H, Yan  L, Zhang  G,  et al.  Association between HLA-B*1301 and dapsone-induced hypersensitivity reactions among leprosy patients in China.  J Invest Dermatol. 2013;133(11):2642-2644.PubMedGoogle ScholarCrossref
16.
Zhang  FR, Liu  H, Irwanto  A,  et al.  HLA-B*13:01 and the dapsone hypersensitivity syndrome.  N Engl J Med. 2013;369(17):1620-1628.PubMedGoogle ScholarCrossref
17.
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):429-437.PubMedGoogle ScholarCrossref
18.
Thakkinstian  A, McElduff  P, D’Este  C, Duffy  D, Attia  J.  A method for meta-analysis of molecular association studies.  Stat Med. 2005;24(9):1291-1306.PubMedGoogle ScholarCrossref
19.
Smits  KM, Schouten  JS, Smits  LJ, Stelma  FF, Nelemans  P, Prins  MH.  A review on the design and reporting of studies on drug-gene interaction.  J Clin Epidemiol. 2005;58(7):651-654.PubMedGoogle ScholarCrossref
20.
Wells  G, Shea  B, O’Connell  D,  et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Posted 2011. Accessed September 24, 2017.
21.
DerSimonian  R, Laird  N.  Meta-analysis in clinical trials.  Control Clin Trials. 1986;7(3):177-188.PubMedGoogle ScholarCrossref
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Higgins  JP, Thompson  SG.  Quantifying heterogeneity in a meta-analysis.  Stat Med. 2002;21(11):1539-1558.PubMedGoogle ScholarCrossref
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Higgins  JP, Thompson  SG, Deeks  JJ, Altman  DG.  Measuring inconsistency in meta-analyses.  BMJ. 2003;327(7414):557-560.PubMedGoogle ScholarCrossref
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Richardus  JH, Smith  TC.  Increased incidence in leprosy of hypersensitivity reactions to dapsone after introduction of multidrug therapy.  Lepr Rev. 1989;60(4):267-273.PubMedGoogle Scholar
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Roujeau  JC, Allanore  L, Liss  Y, Mockenhaupt  M.  Severe cutaneous adverse reactions to drugs (SCAR): definitions, diagnostic criteria, genetic predisposition.  Zhonghua Pifuke Yixue Zazhi. 2009;27:203-209.Google Scholar
26.
González-Galarza  FF, Takeshita  LY, Santos  EJ,  et al.  Allele frequency net 2015 update: new features for HLA epitopes, KIR and disease and HLA adverse drug reaction associations.  Nucleic Acids Res. 2015;43(Database issue):D784-D788.PubMedGoogle ScholarCrossref
27.
Allele Frequency Net Database. The Allele Frequency Net Database. http://www.allelefrequencies.net. Updated January 4, 2015. Accessed September 30, 2017.
28.
Watanabe  H, Watanabe  Y, Tashiro  Y,  et al.  A docking model of dapsone bound to HLA-B*13:01 explains the risk of dapsone hypersensitivity syndrome.  J Dermatol Sci. 2017;88(3):320-329.PubMedGoogle ScholarCrossref
Original Investigation
April 2018

Association Between HLA-B*1301 and Dapsone-Induced Cutaneous Adverse Drug Reactions: A Systematic Review and Meta-analysis

Author Affiliations
  • 1Center of Excellence for Environmental Health and Toxicology, Faculty of Pharmaceutical Sciences, Naresuan University, Phitsanulok, Thailand
  • 2Department of Pharmacy Practice, Faculty of Pharmaceutical Sciences, Naresuan University, Phitsanulok, Thailand
  • 3Pharmacokinetic Research Unit, Faculty of Pharmaceutical Sciences, Naresuan University, Phitsanulok, Thailand
JAMA Dermatol. 2018;154(4):441-446. doi:10.1001/jamadermatol.2017.6484
Key Points

Question  Is HLA-B*1301 genotype associated with dapsone-induced cutaneous adverse reactions?

Findings  In this systematic review and meta-analysis of 3 studies that included 111 patients with dapsone-induced cutaneous adverse drug reactions, 1165 dapsone-tolerant patients, and 3026 healthy controls, a statistically significant association between HLA-B*1301 and dapsone-induced cutaneous adverse reactions was found.

Meaning  Because HLA-B*1301 is associated with dapsone-induced cutaneous adverse reactions, genetic screening for HLA-B*1301 before initiating dapsone therapy is warranted.

Abstract

Importance  Dapsone-induced hypersensitivity syndrome (DHS) is a life-threatening adverse drug reaction. Based on available epidemiologic studies, HLA genotypes may play an important role in DHS.

Objective  To assess the association between HLA-B*1301 and dapsone-induced cutaneous adverse drug reactions (cADRs).

Data Sources  Human studies investigating associations between HLA-B*1301 and dapsone-induced cADRs were systematically searched without language restriction from the inception of each database until September 12, 2017, in PubMed, the Human Genome Epidemiology Network), and the Cochrane Library. Combinations of HLA genotypes, dapsone, and synonymous terms were used; reference lists were searched in selected articles.

Study Selection  Two reviewers identified studies investigating the associations between HLA-B*1301 and dapsone-induced cADRs that reported sufficient data for calculating the frequency of HLA-B*1301 carriers among case and control patients, in which all patients received dapsone before HLA-B*1301 screening. An initial search of the databases identified 391 articles, of which 3 studies (2 in Chinese populations and 1 in a Thai population) met the inclusion criteria.

Data Extraction and Synthesis  Overall odds ratios (ORs) with 95% CIs were calculated using a random-effects model to determine the association between HLA-B*1301 and dapsone-induced cADRs. Subgroup analyses by type of cADR were also performed. PRISMA guidelines were used to abstract and assess data.

Main Outcomes and Measures  Primary outcomes were associations between HLA-B*1301 and dapsone-induced cADRs in dapsone-tolerant controls. The outcomes are reported as overall OR. Statistical heterogeneity was assessed using the Q statistic and I2 tests.

Results  From the 3 included studies, there were 111 unique patients with dapsone-induced cADRs (subsequently used in the meta-analysis), 1165 dapsone-tolerant patients, and 3026 healthy controls. The cases included 64 men and 49 women (2 patients were missing from the meta-analysis; 1 each from 2 of the 3 studies); mean age was 39.7 years. An association between HLA-B*1301 and dapsone-induced cADRs was identified (summary OR, 43.0; 95% CI, 24.0-77.2). Subgroup analyses among types of cADRs produced similar findings in DHS (OR, 51.7; 95% CI, 16.9-158.5), dapsone-induced severe cADRs (Stevens-Johnson syndrome and toxic epidermal necrolysis [SJS/TEN] plus drug rash [adverse skin reaction to a drug] along with eosinophilia and systemic symptoms [DRESS]) (OR, 54.0; 95% Cl, 8.0-366.2), dapsone-induced SJS/TEN (OR, 40.5; 95% CI, 2.8-591.0), and dapsone-induced DRESS (OR, 60.8; 95% CI, 7.4-496.2). There was no heterogeneity (I2 = 0%, P = .38).

Conclusions and Relevance  Associations between HLA-B*1301 and dapsone-induced cADRs were found in dapsone-tolerant and healthy control groups. For patient safety, genetic screening for HLA-B*1301 in Asian populations before dapsone therapy is warranted.

Introduction

Dapsone is an antimicrobial anti-inflammatory drug widely used in the treatment of some diseases.1 As an antimicrobial agent, dapsone has been used to treat leprosy and actinomycetoma and for prophylaxis and treatment of Pneumocystis carinii pneumonia and malaria. It has also been used as an anti-inflammatory agent to treat dermatologic conditions, including dermatitis herpetiformis, linear IgA dermatosis, and pustular psoriasis.2,3 Dapsone has pharmacologic (eg, hemolytic anemia, methemoglobinemia, and agranulocytosis) and idiosyncratic (dapsone-induced hypersensitivity syndrome [DHS]) adverse effects.1Quiz Ref ID Idiosyncratic adverse effects of dapsone range from mild cutaneous reactions to severe life-threatening reactions, such as exfoliated dermatitis, liver failure, agranulocytosis, Stevens-Johnson syndrome and toxic epidermal necrolysis (SJS/TEN), nephritis, and renal failure.4,5 Dapsone-induced hypersensitivity syndrome is a life-threatening drug reaction with a mortality rate of 9.9% to 12.5%.6-8 It is characterized by fever, adverse skin reaction to a drug, and systematic involvement and usually manifests in the first 6 weeks after dapsone treatment initiation. However, Quiz Ref IDHLA genotypes are a family of genes involved in immune reactions. HLA genotypes are the most polymorphic gene cluster in the human genome.9,10 Specific polymorphisms in HLA genotypes are associated with various adverse drug reactions, for example, HLA-B*5801 and allopurinol-induced SJS/TEN,11HLA-B*5701 and abacavir-induced hypersensitivity,12HLA-B*1502 and carbamazepine-induced SJS/TEN,13 and HLA-B*1502 and oxcarbazepine-induced SJS/TEN.14

Associations between HLA genotypes and dapsone-induced cutaneous adverse drug reactions (cADRs) have been investigated in epidemiologic studies.15-17 We aimed to summarize and elucidate the associations between HLA-B*1301 and dapsone-induced cADRs using systematic review and meta-analysis techniques.

Methods
Search Strategy and Selection Criteria

A systematic literature search in PubMed, the Human Genome Epidemiology Network (HuGENet), and the Cochrane Library was performed from database inception until September 2017. Our search terms were combinations of keywords and synonyms for HLA genotypes and dapsone without language or study-design restrictions. Only human studies were included. Additional studies were retrieved from references listed in the included articles. We independently screened titles, abstracts, or both for relevance; studies deemed relevant underwent full-text article assessments for inclusion. Studies were included for case and control groups if (1) HLA-B*1301 and dapsone-induced cADR associations were investigated; (2) all patients received dapsone before HLA-B*1301 screening; and (3) sufficient data to calculate frequency of HLA-B*1301 carriers were reported. If 2 or more studies shared the same population, the study with more complete data or larger sample size was included. For studies that met inclusion criteria but did not provide sufficient data for meta-analysis, we contacted corresponding authors for additional information. This additional information was not included in the present analysis.

The PRISMA guidelines were used to abstract and assess data. We extracted data by study design; eligibility criteria, definition, and diagnostic criteria for cases and controls; patient demographics; dose and duration of dapsone exposure; HLA genotyping technique; and Hardy-Weinberg equilibrium information. The frequency of genotypes was examined by the Hardy-Weinberg equilibrium to determine whether patients from the selected studies were representative of the population.18,19 The Newcastle-Ottawa scale was used to determine the quality of the selected studies.20 Throughout the study, disagreements between reviewers were resolved through discussion until consensus was reached.

Statistical Analysis

The included studies demonstrating associations between HLA-B*1301 and dapsone-induced cADRs were characterized and summarized based on the most recent data. Overall odds ratios (ORs) with 95% CIs were calculated to determine associations between HLA-B*1301 and dapsone-induced cADRs. All analyses were performed using the DerSimonian and Laird method under a random-effects model.21 Analyses were also performed separately on studies using different types of control patients (eg, dapsone-tolerant or healthy controls) and different types of cADRs. Statistical heterogeneity was assessed using the Q statistic and I2 tests.22 Two-sided P ≤ .10 indicated a statistically significant heterogeneity between studies. Heterogeneity I2 values of 25%, 50%, and 75% denote low, moderate, and high heterogeneity across studies, respectively.23 All statistical analyses were performed using R, version 3.4.0 (R Foundation for Statistical Computing).

Results
Search Strategy and Selection Criteria

Our literature search strategy and study selection process are summarized in Figure 1. The initial search of the databases identified 391 articles. After duplicate records were removed, 365 articles were screened on the basis of title, abstract, or both to determine eligibility. Three articles15-17 met inclusion criteria. No additional articles were identified in the bibliographies of the included studies.

Study Characteristics and Quality Assessment

Characteristics of the included studies are summarized in Table 1. All of the included studies15-17 were case-control studies. One hundred eleven unique case patients with dapsone-induced cADRs,15-17 1165 dapsone-tolerant controls,15-17 and 3026 healthy controls15-17 were included in our systematic review and meta-analysis. Mean age of included patients was 39.7 years in case patients,15-17 32.2 years in dapsone-tolerant control patients,15,16 and 39.5 years in healthy controls.15 Because some of the selected studies in this meta-analysis did not provide individual data points, SDs could not be calculated from the available information. Male patients made up 64 of 113 cases (56.6%)15-17 (2 patients were missing from the meta-analysis; 1 each from the study by Wang et al15 and Zhang et al16), 817 of 1144 dapsone-tolerant controls (71.4%),15,16 and 53 of 100 healthy controls (53.0%).15 The mean dose of dapsone was 94.5 mg/d (range, 2-100 mg/d).17 Mean duration of dapsone-induced cADRs was 30.4 days (range, 1-53 days).15,16 All included studies15-17 were conducted in Asian populations (2 in Chinese populations15,16 and 1 in a Thai population17). The studies by Wang et al15 and Zhang et al16 investigated the association between HLA-B*1301 and DHS, whereas Tempark et al17 investigated the association between HLA-B*1301 and dapsone-induced severe cADRs. Diagnostic criteria for DHS, SJS/TEN, and DRESS for each study are summarized in Table 1. The included studies identified HLA genotypes by using polymerase chain reaction sequence-specific primers,15 polymerase chain reaction next-generation sequencing,16 and polymerase chain reaction sequence-specific oligonucleotide primers.17 In the study by Zhang et al,16 reported controls deviated significantly from the Hardy-Weinberg equilibrium (P < 10−8). The mean score of quality assessment using the Newcastle-Ottawa scale for case-control studies was 6.3 (range, 5-7) (Table 1).

Statistical Analysis
Analysis Using Dapsone-Tolerant Control Studies

The associations between HLA-B*1301 and dapsone-induced cADRs are summarized in Table 2. Quiz Ref IDOne hundred eleven patients had dapsone-induced cADRs and 1165 were dapsone tolerant. In these studies, 95 cases and 157 controls carried at least 1 HLA-B*1301 allele. We found an association between HLA-B*1301 and dapsone-induced cADRs (summary OR, 43.0; 95% CI, 24.0-77.2). There was no heterogeneity (I2 = 0%, P = .38) (Table 2 and Figure 2).

In a subgroup analysis by type of cADR, ORs were 51.7 (95% CI, 16.9-158.5; I2 = 46%; P = .17) in the DHS group; 54.0 (95% CI, 8.0-366.2) in the dapsone-induced severe cADRs (SJS/TEN plus DRESS) group; 40.5 (95% CI, 2.8-591.0) in the dapsone-induced SJS/TEN group; and 60.8 (95% CI, 7.4-496.0) in the dapsone-induced DRESS group (Table 2).

Analysis Using Healthy Control Studies

There were 100 patients with dapsone-induced cADRs and 3026 healthy controls. In these studies, 95 cases and 39 controls carried at least 1 HLA-B*1301 allele. Statistically significant associations between HLA-B*1301 and dapsone-induced cADRs were identified (Table 2).

Discussion

To our knowledge, this is the first systematic review and meta-analysis to identify the associations between HLA-B*1301 and dapsone-induced cADRs. An association was found between the HLA-B*1301 genotype and dapsone-induced cADRs (summary OR, 43.0; 95% CI, 24.0-77.2) (Figure 2). This statistically significant association was similar to the results of the subgroup analyses in the DHS, dapsone-induced severe cADRs (SJS/TEN plus DRESS), dapsone-induced SJS/TEN, and dapsone-induced DRESS groups (Table 2). In addition, the association between HLA-B*1301 and dapsone-induced cADRs was found in healthy controls. In the healthy control group, there were duplicate cases in Zhang et al.16 Therefore, summary ORs could not be calculated and this study was not included in the meta-analysis. However, the observed ORs as shown in Table 2 are still relatively high.

Quiz Ref IDAllele frequency of HLA-B*1301 (ƒ) was 0 to 0.019 in European patients, 0.021 in Korean patients, and 0 to 0.015 in Japanese patients. This allele is more prevalent among Chinese (ƒ = 0.009-0.211) and Southeast Asian (ƒ = 0.091-0.021) populations.26,27 Prevalence of HLA-B*1301 is higher in Papua New Guinean (ƒ = 0.283-0.132) and Australian Aboriginal (ƒ = 0.132-0.270) populations.26,27 Nonetheless, outcomes of the dapsone-induced cADRs among persons of other races/ethnicities carrying HLA-B*1301 might be different from those in Chinese and Southeast Asian populations.

Our study demonstrated associations between HLA-B*1301 and dapsone-induced DHS in 2 Chinese populations15,16 and between HLA-B*1301 and dapsone-induced severe cADRs (SJS/TEN plus DRESS) in 1 Thai population.17 To identify any association between HLA-B*1301 and dapsone-induced cADRs in other populations from other geographic areas, future studies are needed.

Quiz Ref IDRecently, a mechanism by which HLA-B*1301 causes DHS was proposed by Watanabe et al.28 Dapsone specifically binds to HLA-B*1301 at the residue Ile95, a proposed binding site called “pocket F.” This specific binding between dapsone and HLA-B*1301 alters the structure of the antigen-recognition site of HLA-B*1301. As a result, the structurally altered protein can recognize its ligands and this leads to the dapsone-induced cADRs.

Limitations

In this report, there were 3 studies in Asian populations (2 studies in Chinese populations and 1 study in a Thai population). Thus, more studies in more diverse populations are needed.

Conclusions

Associations between HLA-B*1301 and dapsone-induced cADRs were identified in both dapsone-tolerant and healthy control groups. Screening for HLA-B*1301 before initiation of dapsone therapy is warranted in Asian populations.

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Article Information

Accepted for Publication: December 24, 2017.

Corresponding Author: Manupat Lohitnavy, PhD, Center of Excellence for Environmental Health and Toxicology, Faculty of Pharmaceutical Sciences, Naresuan University, Phitsanulok 65000, Thailand (manupatl@gmail.com).

Published Online: March 14, 2018. doi:10.1001/jamadermatol.2017.6484

Author Contributions: Both authors had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Both authors.

Acquisition, analysis, or interpretation of data: Both authors.

Drafting of the manuscript: Both authors.

Critical revision of the manuscript for important intellectual content: Both authors.

Statistical analysis: Both authors.

Administrative, technical, or material support: Lohitnavy.

Study supervision: Lohitnavy.

Conflict of Interest Disclosures: None reported.

References
1.
Zhu  YI, Stiller  MJ.  Dapsone and sulfones in dermatology: overview and update.  J Am Acad Dermatol. 2001;45(3):420-434.PubMedGoogle ScholarCrossref
2.
Kannan  G, Vasantha  J, Rani  NV,  et al.  Drug usage evaluation of dapsone.  Indian J Pharm Sci. 2009;71(4):456-460.PubMedGoogle ScholarCrossref
3.
Wozel  G, Blasum  C.  Dapsone in dermatology and beyond.  Arch Dermatol Res. 2014;306(2):103-124.PubMedGoogle ScholarCrossref
4.
Kosseifi  SG, Guha  B, Nassour  DN, Chi  DS, Krishnaswamy  G.  The dapsone hypersensitivity syndrome revisited: a potentially fatal multisystem disorder with prominent hepatopulmonary manifestations.  J Occup Med Toxicol. 2006;1:9.PubMedGoogle ScholarCrossref
5.
Vinod  KV, Arun  K, Dutta  TK.  Dapsone hypersensitivity syndrome: a rare life threatening complication of dapsone therapy.  J Pharmacol Pharmacother. 2013;4(2):158-160.PubMedGoogle ScholarCrossref
6.
Lorenz  M, Wozel  G, Schmitt  J.  Hypersensitivity reactions to dapsone: a systematic review.  Acta Derm Venereol. 2012;92(2):194-199.PubMedGoogle ScholarCrossref
7.
Tian  W, Shen  J, Zhou  M, Yan  L, Zhang  G.  Dapsone hypersensitivity syndrome among leprosy patients in China.  Lepr Rev. 2012;83(4):370-377.PubMedGoogle Scholar
8.
Pandey  B, Shrestha  K, Lewis  J, Hawksworth  RA, Walker  SL.  Mortality due to dapsone hypersensitivity syndrome complicating multi-drug therapy for leprosy in Nepal.  Trop Doct. 2007;37(3):162-163.PubMedGoogle ScholarCrossref
9.
Chung  WH, Hung  SI, Chen  YT.  Human leukocyte antigens and drug hypersensitivity.  Curr Opin Allergy Clin Immunol. 2007;7(4):317-323.PubMedGoogle ScholarCrossref
10.
Bharadwaj  M, Illing  P, Kostenko  L.  Personalized medicine for HLA-associated drug-hypersensitivity reactions.  Per Med. 2010;7(5):495-516. doi:10.2217/pme.10.46Google ScholarCrossref
11.
Somkrua  R, Eickman  EE, Saokaew  S, Lohitnavy  M, Chaiyakunapruk  N.  Association of HLA-B*5801 allele and allopurinol-induced Stevens Johnson syndrome and toxic epidermal necrolysis: a systematic review and meta-analysis.  BMC Med Genet. 2011;12:118.PubMedGoogle ScholarCrossref
12.
Tangamornsuksan  W, Lohitnavy  O, Kongkaew  C,  et al.  Association of HLA-B*5701 genotypes and abacavir-induced hypersensitivity reaction: a systematic review and meta-analysis.  J Pharm Pharm Sci. 2015;18(1):68-76.PubMedGoogle ScholarCrossref
13.
Tangamornsuksan  W, Chaiyakunapruk  N, Somkrua  R, Lohitnavy  M, Tassaneeyakul  W.  Relationship between the HLA-B*1502 allele and carbamazepine-induced Stevens-Johnson syndrome and toxic epidermal necrolysis: a systematic review and meta-analysis.  JAMA Dermatol. 2013;149(9):1025-1032.PubMedGoogle ScholarCrossref
14.
Chen  CB, Hsiao  YH, Wu  T,  et al; Taiwan Severe Cutaneous Adverse Reaction Consortium.  Risk and association of HLA with oxcarbazepine-induced cutaneous adverse reactions in Asians.  Neurology. 2017;88(1):78-86.PubMedGoogle ScholarCrossref
15.
Wang  H, Yan  L, Zhang  G,  et al.  Association between HLA-B*1301 and dapsone-induced hypersensitivity reactions among leprosy patients in China.  J Invest Dermatol. 2013;133(11):2642-2644.PubMedGoogle ScholarCrossref
16.
Zhang  FR, Liu  H, Irwanto  A,  et al.  HLA-B*13:01 and the dapsone hypersensitivity syndrome.  N Engl J Med. 2013;369(17):1620-1628.PubMedGoogle ScholarCrossref
17.
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):429-437.PubMedGoogle ScholarCrossref
18.
Thakkinstian  A, McElduff  P, D’Este  C, Duffy  D, Attia  J.  A method for meta-analysis of molecular association studies.  Stat Med. 2005;24(9):1291-1306.PubMedGoogle ScholarCrossref
19.
Smits  KM, Schouten  JS, Smits  LJ, Stelma  FF, Nelemans  P, Prins  MH.  A review on the design and reporting of studies on drug-gene interaction.  J Clin Epidemiol. 2005;58(7):651-654.PubMedGoogle ScholarCrossref
20.
Wells  G, Shea  B, O’Connell  D,  et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Posted 2011. Accessed September 24, 2017.
21.
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