Immunogenetic Profiling of SLE and LN among Jordanian Patients
Abstract
:1. Introduction
2. Materials and Methods
2.1. Subject Selection
2.2. DNA Extraction and HLA Genotyping
2.3. Statistical Analysis
3. Results
3.1. Demographic Data of the Participants
3.2. HLA-DRB1 Allele Frequencies among SLE Patients and Healthy Controls
3.3. HLA-DQB1 Allele Frequencies among SLE Patients and Healthy Controls
3.4. HLA-DRB1/DQB1 Haplotypes among SLE Patients and Healthy Controls
3.5. HLA-DRB1 Allele Frequencies among SLE Patients with LN and Healthy Controls
3.6. HLA-DQB1 Allele Frequencies among SLE Patients with LN and Healthy Controls
3.7. HLA-DRB1/DQB1 Haplotype Frequencies among SLE Patients with LN and Healthy Controls
3.8. HLA-DRB1 and -DQB1 Allele and Haplotype Frequencies among SLE Patients without LN and SLE with LN
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Xue, K.; Niu, W.Q.; Cui, Y. Association of HLA-DR3 and HLA-DR15 Polymorphisms with Risk of Systemic Lupus Erythematosus. Chin. Med. J. 2018, 131, 2844–2851. [Google Scholar] [CrossRef] [PubMed]
- Goulielmos, G.N.; Zervou, M.I.; Vazgiourakis, V.M.; Ghodke-Puranik, Y.; Garyfallos, A.; Niewold, T.B. The Genetics and Molecular Pathogenesis of Systemic Lupus Erythematosus (SLE) in Populations of Different Ancestry. Gene 2018, 668, 59–72. [Google Scholar] [CrossRef] [PubMed]
- Barber, M.R.W.; Drenkard, C.; Falasinnu, T.; Hoi, A.; Mak, A.; Kow, N.Y.; Svenungsson, E.; Peterson, J.; Clarke, A.E.; Ramsey-Goldman, R. Global Epidemiology of Systemic Lupus Erythematosus. Nat. Rev. Rheumatol. 2021, 17, 515–532. [Google Scholar] [CrossRef] [PubMed]
- Fortuna, G.; Brennan, M.T. Systemic Lupus Erythematosus. Epidemiology, Pathophysiology, Manifestations, and Management. Dent. Clin. N. Am. 2013, 57, 631–655. [Google Scholar] [CrossRef]
- Buniello, A.; Macarthur, J.A.L.; Cerezo, M.; Harris, L.W.; Hayhurst, J.; Malangone, C.; McMahon, A.; Morales, J.; Mountjoy, E.; Sollis, E.; et al. The NHGRI-EBI GWAS Catalog of Published Genome-Wide Association Studies, Targeted Arrays and Summary Statistics 2019. Nucleic Acids Res. 2019, 47, D1005–D1012. [Google Scholar] [CrossRef] [Green Version]
- Kwon, Y.; Chun, S.; Kim, K.; Mak, A. An Update on the Genetics of Systemic Lupus Erythematosus. Cells 2019, 8, 1180. [Google Scholar] [CrossRef] [Green Version]
- Morris, D.L.; Sheng, Y.; Zhang, Y.; Wang, Y.F.; Zhu, Z.; Tombleson, P.; Chen, L.; Cunninghame Graham, D.S.; Bentham, J.; Roberts, A.L.; et al. Genome-Wide Association Meta-Analysis in Chinese and European Individuals Identifies Ten New Loci Associated with Systemic Lupus Erythematosus. Nat. Genet. 2016, 48, 940–946. [Google Scholar] [CrossRef]
- Graham, R.R.; Ortmann, W.A.; Langefeld, C.D.; Jawaheer, D.; Selby, S.A.; Rodine, P.R.; Baechler, E.C.; Rohlf, K.E.; Shark, K.B.; Espe, K.J.; et al. Visualizing Human Leukocyte Antigen Class II Risk Haplotypes in Human Systemic Lupus Erythematosus. Am. J. Hum. Genet. 2002, 71, 543–553. [Google Scholar] [CrossRef] [Green Version]
- Barcellos, L.F.; May, S.L.; Ramsay, P.P.; Quach, H.L.; Lane, J.A.; Nititham, J.; Noble, J.A.; Taylor, K.E.; Quach, D.L.; Chung, S.A.; et al. High-Density SNP Screening of the Major Histocompatibility Complex in Systemic Lupus Erythematosus Demonstrates Strong Evidence for Independent Susceptibility Regions. PLoS Genet. 2009, 5, e1000696. [Google Scholar] [CrossRef]
- Cusick, M.F.; Libbey, J.E.; Fujinami, R.S. Molecular Mimicry as a Mechanism of Autoimmune Disease. Clin. Rev. Allergy Immunol. 2012, 42, 102–111. [Google Scholar] [CrossRef]
- Kim, K.; Bang, S.Y.; Lee, H.S.; Okada, Y.; Han, B.; Saw, W.Y.; Teo, Y.Y.; Bae, S.C. The HLA-DRβ1 Amino Acid Positions 11-13-26 Explain the Majority of SLE-MHC Associations. Nat. Commun. 2014, 5, 5902. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Molineros, J.E.; Looger, L.L.; Kim, K.; Okada, Y.; Terao, C.; Sun, C.; Zhou, X.J.; Raj, P.; Kochi, Y.; Suzuki, A.; et al. Amino Acid Signatures of HLA Class-I and II Molecules Are Strongly Associated with SLE Susceptibility and Autoantibody Production in Eastern Asians. PLoS Genet. 2019, 15, e1008092. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Morris, D.L.; Taylor, K.E.; Fernando, M.M.; Nititham, J.; Alarcón-Riquelme, M.E.; Barcellos, L.F.; Behrens, T.W.; Cotsapas, C.; Gaffney, P.M.; Graham, R.R.; et al. Unraveling Multiple MHC Gene Associations with Systemic Lupus Erythematosus: Model Choice Indicates a Role for HLA Alleles and Non-HLA Genes in Europeans. Am. J. Hum. Genet. 2012, 91, 778–793. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bentham, J.; Morris, D.L.; Cunninghame Graham, D.S.; Pinder, C.L.; Tombleson, P.; Behrens, T.W.; Martín, J.; Fairfax, B.P.; Knight, J.C.; Chen, L.; et al. Genetic Association Analyses Implicate Aberrant Regulation of Innate and Adaptive Immunity Genes in the Pathogenesis of Systemic Lupus Erythematosus. Nat. Genet. 2015, 47, 1457–1464. [Google Scholar] [CrossRef]
- Shimane, K.; Kochi, Y.; Suzuki, A.; Okada, Y.; Ishii, T.; Horita, T.; Saito, K.; Okamoto, A.; Nishimoto, N.; Myouzen, K.; et al. An Association Analysis of HLA-DRB1 with Systemic Lupus Erythematosus and Rheumatoid Arthritis in a Japanese Population: Effects of *09:01 Allele on Disease Phenotypes. Rheumatology 2013, 52, 1172–1182. [Google Scholar] [CrossRef] [Green Version]
- Sun, C.; Molineros, J.E.; Looger, L.L.; Zhou, X.; Okada, Y.; Ma, J.; Qi, Y.; Kim-Howard, X.; Bhattarai, K.; Adler, A.; et al. High-Density Genotyping of Immune-Related Loci Identifies New SLE Risk Variants in Individuals with Asian Ancestry. Nat. Genet. 2016, 48, 323–330. [Google Scholar] [CrossRef] [Green Version]
- Zhang, J.; Zhan, W.; Yang, B.; Tian, A.; Chen, L.; Liao, Y.; Wu, Y.; Cai, B.; Wang, L. Genetic Polymorphisms of Rs3077 and Rs9277535 in HLA-DP Associated with Systemic Lupus Erythematosus in a Chinese Population. Sci. Rep. 2017, 7, 39757. [Google Scholar] [CrossRef] [Green Version]
- Hachicha, H.; Kammoun, A.; Mahfoudh, N.; Marzouk, S.; Feki, S.; Fakhfakh, R.; Fourati, H.; Haddouk, S.; Frikha, F.; Gaddour, L.; et al. Human Leukocyte Antigens-DRB1*03 Is Associated with Systemic Lupus Erythematosus and Anti-SSB Production in South Tunisia. Int. J. Health Sci. 2018, 12, 21–27. [Google Scholar]
- Mokbel, A.N.; Al-Zifzaf, D.S.; ElSawy, W.S.; ElGabarty, S. Association of HLA-DQB1*06 with Susceptibility to Systemic Lupus Erythematosus in Egyptians. Egypt. Rheumatol. 2015, 37, 17–22. [Google Scholar] [CrossRef] [Green Version]
- Langefeld, C.D.; Ainsworth, H.C.; Graham DS, C.; Kelly, J.A.; Comeau, M.E.; Marion, M.C.; Howard, T.D.; Ramos, P.S.; Croker, J.A.; Morris, D.L.; et al. Transancestral Mapping and Genetic Load in Systemic Lupus Erythematosus. Nat. Commun. 2017, 8, 16021. [Google Scholar] [CrossRef] [Green Version]
- Aringer, M.; Costenbader, K.; Daikh, D.; Brinks, R.; Mosca, M.; Ramsey-Goldman, R.; Smolen, J.S.; Wofsy, D.; Boumpas, D.T.; Kamen, D.L.; et al. 2019 European League Against Rheumatism/American College of Rheumatology Classification Criteria for Systemic Lupus Erythematosus. Ann. Rheum. Dis. 2019, 78, 1151–1159. [Google Scholar] [CrossRef] [PubMed]
- Jarrar, Y.B.; Ghishan, M. The Nudix Hydrolase 15 (NUDT15) Gene Variants among Jordanian Arab Population. Asian Pac. J. Cancer Prev. 2019, 20, 801–808. [Google Scholar] [CrossRef] [PubMed]
- Khdair, S.I.; Jarrar, Y.B.; Jarrar, W. Immunogenetic Prediction of VDR Gene SNPs: Lack of Association with Susceptibility to Type 1 Diabetes in Jordanian Patients. Diabetes Metab. Syndr. Obes. Targets Ther. 2021, 14, 4079–4087. [Google Scholar] [CrossRef] [PubMed]
- Weber, F.; Knapp, G.; Ickstadt, K.; Kundt, G.; Glass, Ä. Zero-Cell Corrections in Random-Effects Meta-Analyses. Res. Synth. Methods 2020, 11, 913–919. [Google Scholar] [CrossRef] [PubMed]
- Ruxton, G.D.; Neuhäuser, M. Review of Alternative Approaches to Calculation of a Confidence Interval for the Odds Ratio of a 2 × 2 Contingency Table. Methods Ecol. Evol. 2013, 4, 9–13. [Google Scholar] [CrossRef]
- MedCalc Software Ltd. Odds Ratio Calculator. Available online: https://www.medcalc.org/calc/odds_ratio.php (accessed on 2 October 2022).
- Schoonjans, F.; Zalata, A.; Depuydt, C.E.; Comhaire, F.H. MedCalc: A New Computer Program for Medical Statistics. Comput. Methods Programs Biomed. 1995, 48, 257–262. [Google Scholar] [CrossRef]
- Ohyama, K.; Sugiura, M. Evaluation of the Association between Topical Prostaglandin F2α Analogs and Asthma Using the Jader Database: Comparison with β-Blockers. Yakugaku Zasshi 2018, 138, 559–564. [Google Scholar] [CrossRef] [Green Version]
- Kawasaki, A.; Hasebe, N.; Hidaka, M.; Hirano, F.; Sada, K.E.; Kobayashi, S.; Yamada, H.; Furukawa, H.; Yamagata, K.; Sumida, T.; et al. Protective Role of HLA-DRB1∗13:02 against Microscopic Polyangiitis and MPO-ANCA-Positive Vasculitides in a Japanese Population: A Case-Control Study. PLoS ONE 2016, 11, e0154393. [Google Scholar] [CrossRef] [Green Version]
- Adwan, M. Clinical and Serologic Characteristics of Systemic Lupus Erythematosus in the Arab World: A Pooled Analysis of 3,273 Patients. Arch. Rheumatol. 2018, 33, 455–463. [Google Scholar] [CrossRef]
- Graham, R.R.; Ortmann, W.; Rodine, P.; Espe, K.; Langefeld, C.; Lange, E.; Williams, A.; Beck, S.; Kyogoku, C.; Moser, K.; et al. Specific Combinations of HLA-DR2 and DR3 Class II Haplotypes Contribute Graded Risk for Disease Susceptibility and Autoantibodies in Human SLE. Eur. J. Hum. Genet. 2007, 15, 823–830. [Google Scholar] [CrossRef] [Green Version]
- Castaño-Rodríguez, N.; Diaz-Gallo, L.M.; Pineda-Tamayo, R.; Rojas-Villarraga, A.; Anaya, J.M. Meta-Analysis of HLA-DRB1 and HLA-DQB1 Polymorphisms in Latin American Patients with Systemic Lupus Erythematosus. Autoimmun. Rev. 2008, 7, 322–330. [Google Scholar] [CrossRef]
- Ayed, K.; Gorgi, Y.; Ayed-Jendoubi, S.; Bardi, R. The Involvement of HLA-DRBI*, DQA1*, DQB1* and Complement C4A Loci in Diagnosing Systemic Lupus Erythermatosus among Tunisians. Ann. Saudi Med. 2004, 24, 31–35. [Google Scholar] [CrossRef]
- Pan, C.F.; Wu, C.J.; Chen, H.H.; Dang, C.W.; Chang, F.M.; Liu, H.F.; Chu, C.C.; Lin, M.; Lee, Y.J. Molecular Analysis of HLA-DRB1 Allelic Associations with Systemic Lupus Erythematous and Lupus Nephritis in Taiwan. Lupus 2009, 18, 698–704. [Google Scholar] [CrossRef]
- Marchini, M.; Antonioli, R.; Lleò, A.; Barili, M.; Caronni, M.; Origgi, L.; Vanoli, M.; Scorza, R. HLA Class II Antigens Associated with Lupus Nephritis in Italian SLE Patients. Hum. Immunol. 2003, 64, 462–468. [Google Scholar] [CrossRef]
- Vasconcelos, C.; Carvalho, C.; Leal, B.; Pereira, C.; Bettencourt, A.; Costa, P.P.; Marinho, A.; Barbosa, P.; Almeida, I.; Farinha, F.; et al. HLA in Portuguese Systemic Lupus Erythematosus Patients and Their Relation to Clinical Features. Ann. N. Y. Acad. Sci. 2009, 1173, 575–580. [Google Scholar] [CrossRef]
- Fernando MM, A.; Stevens, C.R.; Sabeti, P.C.; Walsh, E.C.; McWhinnie AJ, M.; Shah, A.; Green, T.; Rioux, J.D.; Vyse, T.J. Identification of Two Independent Risk Factors for Lupus within the MHC in United Kingdom Families. PLoS Genet. 2007, 3, 2109–2121. [Google Scholar] [CrossRef]
- Hussain, N.; Jaffery, G.; Sabri, A.N.; Hasnain, S. HLA Association in SLE Patients from Lahore-Pakistan. Bosn. J. Basic Med. Sci. 2011, 11, 20–26. [Google Scholar] [CrossRef] [Green Version]
- Farivar, S.; Tezerjani, M.D.; Shiari, R. Association of HLA-DRB1 Alleles with Juvenile-Onset Systemic Lupus Erythematosus (SLE) in Iranian Children. Int. J. Pediatr. 2015, 3, 555–560. [Google Scholar] [CrossRef]
- Dedhia, L.; Pradhan, V.; Ghosh, K.; Nadkar, M.; Parekh, S. Association of Human Leucocyte Antigen (HLA) Class II with Systemic Lupus Erythematosis (SLE) Patients from Western India. Meta Gene 2018, 16, 230–233. [Google Scholar] [CrossRef]
- Rezaieyazdi, Z.; Tavakkol-Afshari, J.; Esmaili, E.; Orouji, E.; Pezeshkpour, F.; Khodadoost, M.; Mazhani, M.; Sandooghi, M. Association of HLA-DQB1 Allelic Sequence Variation with Susceptibility to Systemic Lupus Erythematosus. Iran. J. Allergy Asthma Immunol. 2008, 7, 91–95. [Google Scholar]
- Kapitany, A.; Tarr, T.; Gyetvai, A.; Szodoray, P.; Tumpek, J.; Poor, G.; Szegedi, G.; Sipka, S.; Kiss, E. Human Leukocyte Antigen-DRB1 and -DQB1 Genotyping in Lupus Patients with and without Antiphospholipid Syndrome. Ann. N. Y. Acad. Sci. 2009, 1173, 545–551. [Google Scholar] [CrossRef] [PubMed]
- Bolin, K.; Sandling, J.K.; Zickert, A.; Jönsen, A.; Sjöwall, C.; Svenungsson, E.; Bengtsson, A.A.; Eloranta, M.L.; Rönnblom, L.; Syvänen, A.C.; et al. Association of STAT4 Polymorphism with Severe Renal Insufficiency in Lupus Nephritis. PLoS ONE 2013, 8, e84450. [Google Scholar] [CrossRef] [PubMed]
- Gunawan, A.; Handono, K.; Kalim, H.; Susianti, H.; Eko, M.H.; Lawrence, G.S.; Hasanah, D.; Mertianti, E.; Candradikusuma, D. The Importance of HLA-DRB1 Alleles in Patients with Lupus Nephritis. Turkish J. Immunol. 2018, 6, 118–122. [Google Scholar] [CrossRef]
- Bhallil, O.; Ibrahimi, A.; Ouadghiri, S.; Ouzeddoun, N.; Benseffaj, N.; Bayahia, R.; Essakalli, M. HLA Class II with Lupus Nephritis in Moroccan Patients. Immunol. Investig. 2017, 46, 1–9. [Google Scholar] [CrossRef]
- Wadi, W.; Elhefny, N.E.A.M.; Mahgoub, E.H.; Almogren, A.; Hamam, K.D.; Al-Hamed, H.A.; Gasim, G.I. Relation between HLA Typing and Clinical Presentations in Systemic Lupus Erythematosus Patients in Al-Qassim Region, Saudi Arabia. Int. J. Health Sci. 2014, 8, 159–165. [Google Scholar] [CrossRef]
- de Holanda, M.I.; Klumb, E.; Imada, A.; Lima, L.A.; Alcântara, I.; Gregório, F.; Christiani, L.F.; Martins, C.O.; Timoner, B.E.; Motta, J.; et al. The Prevalence of HLA Alleles in a Lupus Nephritis Population. Transpl. Immunol. 2018, 47, 37–43. [Google Scholar] [CrossRef]
- Niu, Z.; Zhang, P.; Tong, Y. Value of HLA-DR Genotype in Systemic Lupus Erythematosus and Lupus Nephritis: A Meta-Analysis. Int. J. Rheum. Dis. 2015, 18, 17–28. [Google Scholar] [CrossRef]
- Xu, R.; Li, Q.; Liu, R.; Shen, J.; Li, M.; Zhao, M.; Wang, M.; Liao, Q.; Mao, H.; Li, Z.; et al. Association Analysis of the MHC in Lupus Nephritis. J. Am. Soc. Nephrol. 2017, 28, 3383–3394. [Google Scholar] [CrossRef] [Green Version]
- Tsokos, G.C. Systemic Lupus Erythematosus. N. Engl. J. Med. 2011, 365, 2110–2121. [Google Scholar] [CrossRef]
Control | SLE | ||||||
---|---|---|---|---|---|---|---|
Allele | n= 148 | (%) | n = 160 | (%) | p Value | OR | 95% CI |
DRB1*0101 | 9 | 6.1 | 2 | 1.3 | 0.022 | 0.20 | 0.04–0.92 |
DRB1*0103 | 2 | 1.4 | 0 | 0 | 0.274 | 0.18 | 0.01–3.83 |
DRB1*0301 | 13 | 8.8 | 32 | 20.0 | 0.005 | 2.60 | 1.30–5.17 |
DRB1*0302 | 0 | 0 | 3 | 1.9 | 0.213 | 6.60 | 0.34–128.9 |
DRB1*0401 | 0 | 0 | 5 | 3.1 | 0.112 | 10.51 | 0.58–191.7 |
DRB1*0402 | 3 | 2.0 | 1 | 0.6 | 0.278 | 0.31 | 0.03–2.96 |
DRB1*0403 | 11 | 7.4 | 0 | 0 | 0.023 | 0.04 | 0.002–0.64 |
DRB1*0405 | 0 | 0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
DRB1*0701 | 26 | 17.6 | 11 | 6.9 | 0.004 | 0.35 | 0.17–0.73 |
DRB1*0801 | 3 | 2.0 | 0 | 0 | 0.178 | 0.13 | 0.01–2.53 |
DRB1*1001 | 8 | 5.4 | 13 | 8.1 | 0.344 | 1.55 | 0.62–3.85 |
DRB1*1101 | 20 | 13.5 | 36 | 22.5 | 0.041 | 1.86 | 1.02–3.39 |
DRB1*1102 | 8 | 5.4 | 21 | 13.1 | 0.020 | 2.64 | 1.13–6.17 |
DRB1*1103 | 0 | 0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
DRB1*1201 | 1 | 0.7 | 4 | 2.5 | 0.206 | 3.77 | 0.42–34.16 |
DRB1*1301 | 13 | 8.8 | 4 | 2.5 | 0.016 | 0.27 | 0.09–0.84 |
DRB1*1302 | 0 | 0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
DRB1*1303 | 7 | 4.7 | 2 | 1.3 | 0.070 | 0.26 | 0.05–1.25 |
DRB1*1401 | 8 | 5.4 | 0 | 0 | 0.042 | 0.05 | 0.003–0.90 |
DRB1*1402 | 0 | 0 | 2 | 1.3 | 0.320 | 4.69 | 0.22–98.39 |
DRB1*1404 | 1 | 0.7 | 0 | 0 | 0.470 | 0.31 | 0.01–7.58 |
DRB1*1501 | 13 | 8.8 | 20 | 12.5 | 0.292 | 1.48 | 0.71–3.10 |
DRB1*1502 | 1 | 0.7 | 0 | 0 | 0.470 | 0.31 | 0.01–7.58 |
DRB1*1601 | 1 | 0.7 | 1 | 0.6 | 0.956 | 0.93 | 0.06–14.92 |
Control | SLE | ||||||
---|---|---|---|---|---|---|---|
Allele | n = 148 | (%) | n = 160 | (%) | p Value | OR | 95% CI |
DQB1*0201 | 33 | 22.3 | 35 | 21.9 | 0.929 | 0.98 | 0.57–1.67 |
DQB1*0202 | 2 | 1.4 | 0 | 0 | 0.274 | 0.18 | 0.01–3.83 |
DQB1*0301 | 38 | 25.7 | 55 | 34.4 | 0.097 | 1.52 | 0.93–2.48 |
DQB1*0302 | 17 | 11.5 | 18 | 11.3 | 0.948 | 0.98 | 0.48–1.98 |
DQB1*0303 | 3 | 2.0 | 2 | 1.3 | 0.590 | 0.61 | 0.10–3.71 |
DQB1*0401 | 0 | 0 | 2 | 1.3 | 0.320 | 4.69 | 0.22–98.39 |
DQB1*0402 | 2 | 1.4 | 2 | 1.3 | 0.937 | 0.92 | 0.13–6.65 |
DQB1*0501 | 24 | 16.2 | 17 | 10.6 | 0.149 | 0.61 | 0.32–1.20 |
DQB1*0502 | 1 | 0.7 | 1 | 0.6 | 0.956 | 0.93 | 0.06–14.92 |
DQB1*0503 | 1 | 0.7 | 0 | 0 | 0.470 | 0.31 | 0.01–7.58 |
DQB1*0601 | 2 | 1.4 | 21 | 13.1 | <0.001 | 11.03 | 2.54–47.91 |
DQB1*0602 | 15 | 10.1 | 7 | 4.4 | 0.050 | 0.41 | 0.16–1.03 |
DQB1*0603 | 10 | 6.8 | 0 | 0 | 0.028 | 0.04 | 0.002–0.71 |
Controls | SLE | ||||||
---|---|---|---|---|---|---|---|
Haplotype | n = 148 | (%) | n = 160 | (%) | p Value | OR | 95% CI |
0101/0201 | 0 | 0 | 2 | 1.3 | 0.320 | 4.69 | 0.22–98.39 |
0101/0301 | 2 | 1.4 | 0 | 0.0 | 0.274 | 0.18 | 0.01–3.83 |
0101/0501 | 7 | 4.7 | 0 | 0.0 | 0.053 | 0.06 | 0.003–1.04 |
0103/0301 | 2 | 1.4 | 0 | 0.0 | 0.274 | 0.18 | 0.01–3.83 |
0301/0201 | 11 | 7.4 | 24 | 15.0 | 0.037 | 2.20 | 1.04–4.66 |
0301/0301 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
0301/0302 | 0 | 0.0 | 4 | 2.5 | 0.151 | 8.54 | 0.46–159.9 |
0301/0303 | 1 | 0.7 | 1 | 0.6 | 0.956 | 0.93 | 0.06–14.92 |
0301/0501 | 1 | 0.7 | 1 | 0.6 | 0.956 | 0.93 | 0.06–14.92 |
0301/0602 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
0302/0402 | 0 | 0.0 | 3 | 1.9 | 0.213 | 6.60 | 0.34–128.9 |
0401/0301 | 0 | 0.0 | 2 | 1.3 | 0.320 | 4.69 | 0.22–98.39 |
0401/0302 | 0 | 0.0 | 3 | 1.9 | 0.213 | 6.60 | 0.34–128.9 |
0402/0302 | 3 | 2.0 | 1 | 0.6 | 0.278 | 0.30 | 0.03–2.96 |
0403/0302 | 9 | 6.1 | 0 | 0.0 | 0.034 | 0.05 | 0.003–0.79 |
0403/0402 | 2 | 1.4 | 0 | 0.0 | 0.274 | 0.18 | 0.01–3.83 |
0405/0401 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
0701/0201 | 24 | 16.2 | 7 | 4.4 | 0.001 | 0.24 | 0.10–0.57 |
0701/0301 | 0 | 0.0 | 2 | 1.3 | 0.320 | 4.69 | 0.22–98.39 |
0701/0303 | 2 | 1.4 | 1 | 0.6 | 0.517 | 0.46 | 0.04–5.12 |
0702/0201 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
0801/0301 | 3 | 2.0 | 0 | 0.0 | 0.178 | 0.13 | 0.01–2.53 |
1001/0201 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
1001/0302 | 2 | 1.4 | 1 | 0.6 | 0.517 | 0.46 | 0.04–5.12 |
1001/0501 | 6 | 4.1 | 10 | 6.3 | 0.386 | 1.58 | 0.56–4.45 |
1001/0602 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
1101/0301 | 18 | 12.2 | 26 | 16.3 | 0.306 | 1.40 | 0.73–2.68 |
1101/0302 | 1 | 0.7 | 5 | 3.1 | 0.120 | 4.74 | 0.55–41.07 |
1101/0501 | 0 | 0.0 | 4 | 2.5 | 0.151 | 8.54 | 0.46–159.9 |
1101/0602 | 1 | 0.7 | 0 | 0.0 | 0.470 | 0.31 | 0.01–7.58 |
1102/0301 | 7 | 4.7 | 17 | 10.6 | 0.054 | 2.40 | 0.96–5.95 |
1102/0302 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
1102/0601 | 0 | 0.0 | 2 | 1.3 | 0.320 | 4.69 | 0.22–98.39 |
1102/0602 | 1 | 0.7 | 2 | 1.3 | 0.608 | 1.86 | 0.17–20.74 |
1103/0201 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
1201/0301 | 1 | 0.7 | 4 | 2.5 | 0.206 | 3.77 | 0.42–34.12 |
1301/0301 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
1301/0302 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
1301/0501 | 3 | 2.0 | 0 | 0.0 | 0.178 | 0.13 | 0.01–2.53 |
1301/0602 | 0 | 0.0 | 2 | 1.3 | 0.320 | 4.69 | 0.22–98.39 |
1301/0603 | 10 | 6.8 | 0 | 0.0 | 0.028 | 0.04 | 0.002–0.71 |
1302/0302 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
1303/0201 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
1303/0301 | 5 | 3.4 | 0 | 0.0 | 0.090 | 0.08 | 0.01–1.48 |
1303/0302 | 2 | 1.4 | 1 | 0.6 | 0.517 | 0.46 | 0.04–5.12 |
1401/0501 | 5 | 3.4 | 0 | 0.0 | 0.090 | 0.08 | 0.01–1.48 |
1401/0602 | 3 | 2.0 | 0 | 0.0 | 0.178 | 0.13 | 0.01–2.53 |
1402/0301 | 0 | 0.0 | 2 | 1.3 | 0.320 | 4.69 | 0.22–98.38 |
1404/0503 | 1 | 0.7 | 0 | 0.0 | 0.470 | 0.31 | 0.01–7.58 |
1501/0201 | 0 | 0.0 | 1 | 0.6 | 0.530 | 2.79 | 0.11–69.10 |
1501/0501 | 1 | 0.7 | 0 | 0.0 | 0.470 | 0.31 | 0.01–7.58 |
1501/0601 | 2 | 1.4 | 19 | 11.9 | <0.001 | 9.84 | 2.25–43.01 |
1501/0602 | 10 | 6.8 | 0 | 0.0 | 0.028 | 0.04 | 0.002–0.71 |
1502/0501 | 1 | 0.7 | 0 | 0.0 | 0.470 | 0.31 | 0.01–7.58 |
1601/0502 | 1 | 0.7 | 1 | 0.6 | 0.956 | 0.93 | 0.06–14.92 |
Control | SLE with Nephritis | ||||||
---|---|---|---|---|---|---|---|
Allele | n = 148 | (%) | n = 78 | (%) | p Value | OR | 95% CI |
DRB1*0101 | 9 | 6.1 | 0 | 0 | 0.104 | 0.09 | 0.01–1.63 |
DRB1*0103 | 2 | 1.4 | 0 | 0 | 0.526 | 0.37 | 0.02–7.87 |
DRB1*0301 | 13 | 8.8 | 17 | 21.8 | 0.006 | 2.89 | 1.32–6.33 |
DRB1*0401 | 0 | 0 | 3 | 3.8 | 0.084 | 13.77 | 0.70–270 |
DRB1*0402 | 3 | 2.0 | 1 | 1.3 | 0.686 | 0.63 | 0.06-6.14 |
DRB1*0403 | 11 | 7.4 | 0 | 0 | 0.076 | 0.08 | 0.004–1.31 |
DRB1*0701 | 26 | 17.6 | 6 | 7.7 | 0.040 | 0.39 | 0.15–1.00 |
DRB1*0801 | 3 | 2.0 | 0 | 0 | 0.382 | 0.26 | 0.01–5.19 |
DRB1*1001 | 8 | 5.4 | 4 | 5.1 | 0.930 | 0.95 | 0.28–3.25 |
DRB1*1101 | 20 | 13.5 | 19 | 24.4 | 0.040 | 2.06 | 1.02–4.15 |
DRB1*1102 | 8 | 5.4 | 8 | 10.3 | 0.176 | 2.00 | 0.72–5.55 |
DRB1*1103 | 0 | 0 | 1 | 1.3 | 0.286 | 5.75 | 0.23–142.8 |
DRB1*1201 | 1 | 0.7 | 2 | 2.6 | 0.238 | 3.87 | 0.35–43.35 |
DRB1*1301 | 13 | 8.8 | 1 | 1.3 | 0.026 | 0.14 | 0.02–1.05 |
DRB1*1302 | 0 | 0 | 1 | 1.3 | 0.286 | 5.75 | 0.23–142.8 |
DRB1*1303 | 7 | 4.7 | 1 | 1.3 | 0.182 | 0.26 | 0.03–2.16 |
DRB1*1401 | 8 | 5.4 | 0 | 0 | 0.124 | 0.11 | 0.01–1.85 |
DRB1*1404 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
DRB1*1501 | 13 | 8.8 | 14 | 17.9 | 0.043 | 2.27 | 1.01–5.11 |
DRB1*1502 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
DRB1*1601 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
Control | SLE with Nephritis | ||||||
---|---|---|---|---|---|---|---|
Allele | n = 148 | (%) | n = 78 | (%) | ρ Value | OR | 95% CI |
DQB1*0201 | 33 | 22.3 | 21 | 26.9 | 0.438 | 1.28 | 0.68–2.42 |
DQB1*0202 | 2 | 1.4 | 0 | 0 | 0.526 | 0.37 | 0.02–7.87 |
DQB1*0301 | 38 | 25.7 | 26 | 33.3 | 0.224 | 1.45 | 0.80–2.63 |
DQB1*0302 | 17 | 11.5 | 8 | 10.3 | 0.779 | 0.88 | 0.36–2.14 |
DQB1*0303 | 3 | 2.0 | 1 | 1.3 | 0.686 | 0.63 | 0.06–6.14 |
DQB1*0402 | 2 | 1.4 | 0 | 0 | 0.526 | 0.37 | 0.02–7.87 |
DQB1*0501 | 24 | 16.2 | 6 | 7.7 | 0.073 | 0.43 | 0.17–1.10 |
DQB1*0502 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
DQB1*0503 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
DQB1*0601 | 2 | 1.4 | 16 | 20.5 | <0.001 | 18.84 | 4.21–84.40 |
DQB1*0602 | 15 | 10.1 | 0 | 0 | 0.044 | 0.06 | 0.003–0.93 |
DQB1*0603 | 10 | 6.8 | 0 | 0 | 0.089 | 0.08 | 0.005–1.45 |
Controls | SLE with Nephritis | - | |||||
---|---|---|---|---|---|---|---|
Haplotype | n = 148 | (%) | n =78 | (%) | p Value | OR | 95% CI |
0101/0301 | 2 | 1.4 | 0 | 0 | 0.526 | 0.37 | 0.02–7.87 |
0101/0501 | 7 | 4.7 | 0 | 0 | 0.149 | 0.12 | 0.01–2.13 |
0103/0301 | 2 | 1.4 | 0 | 0 | 0.526 | 0.37 | 0.02–7.87 |
0301/0201 | 11 | 7.4 | 13 | 16.7 | 0.032 | 2.50 | 1.06–5.86 |
0301/0301 | 0 | 0.0 | 1 | 1.3 | 0.286 | 5.75 | 0.23–142.80 |
0301/0302 | 0 | 0.0 | 2 | 2.6 | 0.144 | 9.71 | 0.46–204.7 |
0301/0303 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
0301/0501 | 1 | 0.7 | 1 | 1.3 | 0.644 | 1.91 | 0.12–30.94 |
0401/0301 | 0 | 0.0 | 2 | 2.6 | 0.144 | 9.71 | 0.46–204.7 |
0401/0302 | 0 | 0.0 | 1 | 1.3 | 0.286 | 5.75 | 0.23–142.80 |
0402/0302 | 3 | 2 | 1 | 1.3 | 0.686 | 0.63 | 0.06–6.14 |
0403/0302 | 9 | 6.1 | 0 | 0 | 0.104 | 0.09 | 0.01–1.63 |
0403/0402 | 2 | 1.4 | 0 | 0 | 0.526 | 0.37 | 0.02–7.87 |
0701/0201 | 24 | 16.2 | 4 | 5.1 | 0.016 | 0.28 | 0.09–0.84 |
0701/0303 | 2 | 1.4 | 1 | 1.3 | 0.965 | 0.95 | 0.09–10.62 |
0702/0201 | 0 | 0.0 | 1 | 1.3 | 0.286 | 5.75 | 0.23–142.80 |
0801/0301 | 3 | 2.0 | 0 | 0 | 0.382 | 0.26 | 0.01–5.19 |
1001/0201 | 0 | 0.0 | 1 | 1.3 | 0.286 | 5.75 | 0.23–142.80 |
1001/0302 | 2 | 1.4 | 0 | 0 | 0.526 | 0.37 | 0.02–7.87 |
1001/0501 | 6 | 4.1 | 3 | 3.8 | 0.939 | 0.95 | 0.23–3.90 |
1101/0301 | 18 | 12.2 | 14 | 17.9 | 0.236 | 1.60 | 0.74–3.38 |
1101/0302 | 1 | 0.7 | 2 | 2.6 | 0.238 | 3.87 | 0.35–43.35 |
1101/0501 | 0 | 0.0 | 2 | 2.6 | 0.144 | 9.71 | 0.46–204.7 |
1101/0602 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
1102/0301 | 7 | 4.7 | 6 | 7.7 | 0.363 | 1.68 | 0.54–5.18 |
1102/0302 | 0 | 0.0 | 1 | 1.3 | 0.286 | 5.75 | 0.23–142.80 |
1102/0602 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
1103/0201 | 0 | 0.0 | 1 | 1.3 | 0.286 | 5.75 | 0.23–142.80 |
1201/0301 | 1 | 0.7 | 2 | 2.6 | 0.238 | 3.87 | 0.35–43.35 |
1301/0501 | 3 | 2.0 | 0 | 0 | 0.382 | 0.26 | 0.01–5.19 |
1301/0603 | 10 | 6.8 | 0 | 0 | 0.089 | 0.08 | 0.01–1.45 |
1303/0301 | 5 | 3.4 | 0 | 0 | 0.227 | 0.17 | 0.01–3.05 |
1302/0302 | 0 | 0.0 | 1 | 1.3 | 0.286 | 5.75 | 0.23–142.80 |
1303/0302 | 2 | 1.4 | 0 | 0 | 0.526 | 0.37 | 0.02–7.87 |
1401/0501 | 5 | 3.4 | 0 | 0 | 0.227 | 0.17 | 0.01–3.05 |
1401/0602 | 3 | 2.0 | 0 | 0 | 0.382 | 0.26 | 0.01–5.19 |
1404/0503 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
1501/0501 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
1501/0601 | 2 | 1.4 | 14 | 17.9 | <0.001 | 15.97 | 3.53–72.32 |
1501/0602 | 10 | 6.8 | 0 | 0 | 0.089 | 0.08 | 0.01–1.45 |
1502/0501 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
1601/0502 | 1 | 0.7 | 0 | 0 | 0.775 | 0.63 | 0.03–15.56 |
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Khdair, S.I.; Al-Bdour, R.; Jarrar, W.; Hammad, A.; Al-Jayeh, A.; Masa’deh, M.; Adwan, M.; Farah, R. Immunogenetic Profiling of SLE and LN among Jordanian Patients. J. Pers. Med. 2022, 12, 1955. https://doi.org/10.3390/jpm12121955
Khdair SI, Al-Bdour R, Jarrar W, Hammad A, Al-Jayeh A, Masa’deh M, Adwan M, Farah R. Immunogenetic Profiling of SLE and LN among Jordanian Patients. Journal of Personalized Medicine. 2022; 12(12):1955. https://doi.org/10.3390/jpm12121955
Chicago/Turabian StyleKhdair, Sawsan I., Rawan Al-Bdour, Wassan Jarrar, Alaa Hammad, Aya Al-Jayeh, Mohammad Masa’deh, Marwan Adwan, and Randa Farah. 2022. "Immunogenetic Profiling of SLE and LN among Jordanian Patients" Journal of Personalized Medicine 12, no. 12: 1955. https://doi.org/10.3390/jpm12121955