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Genetic Heterogeneity of Beta Thalassemia in Lebanon Reflects

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Genetic Heterogeneity of Beta Thalassemia in Lebanon Reflects doi: 10.1046/j.1529-8817.2004.00138.x Genetic Heterogeneity of Beta Thalassemia in Lebanon Reflects Historic and Recent Population Migration N. J. Makhoul1,R.S.Wells2,H.Kaspar1,3,H.Shbaklo3,A.Taher1,4,N.Chakar1 and P. A. Zalloua1,5∗ 1Department of Obstetrics and Gynecology, American University of Beirut, Beirut, Lebanon 2Oxford University, London, UK 3Genetics Research Laboratory, Chronic Care Center, Beirut, Lebanon 4Department of Internal Medicine, American University of Beirut, Beirut, Lebanon 5Program for Population Genetics, Harvard School of Public Health, Boston, USA Summary Beta thalassemia is an autosomal recessive disorder characterized by reduced (β+)orabsent (β0) beta-globin chain synthesis. In Lebanon it is the most predominant genetic defect. In this study we investigated the religious and geographic distribution of the β-thalassemia mutations identified in Lebanon, and traced their precise origins. A total of 520 β-globin chromosomes from patients of different religious and regional backgrounds was studied. Beta thalassemia mutations were identified using Amplification Refractory Mutation System (ARMS) PCR or direct gene sequencing. Six (IVS-I-110, IVS-I-1, IVS-I-6, IVS-II-1, cd 5 and the C>T substitution at cd 29) out of 20 β-globin defects identified accounted for more than 86% of the total β-thalassemia chromosomes. Sunni Muslims had the highest β-thalassemia carrier rate and presented the greatest heterogeneity, with 16 different mutations. Shiite Muslims followed closely with 13 mutations, whereas Maronites represented 11.9% of all β-thalassemic subjects and carried 7 different mutations. RFLP haplotype analysis showed that the observed genetic diversity originated from both new mutational events and gene flow from population migration. This study provides information about the types and distribution of β-thalassemia mutations within each religious group and geographic region, which is essential for the implementation of screening and prevention programs. Introduction are genetically protected against malaria and therefore selectively advantaged (Haldane, 1949). Beta thalassemia is an autosomal recessive disorder char- Although over 300 different mutations in the β- acterized by reduced (β+)orabsent (β0) beta-globin globin gene have been described (Huisman et al. 1997), chain synthesis (Weatherall & Clegg, 1981). The disor- each population or ethnic group has been found to have der is manifested by severe hemolytic anemia, requiring its own characteristic set of mutations. Identification aregular blood transfusion and iron chelation therapy. of both common and rare β-thalassemia mutations has Beta thalassemia occurs with high frequency in areas proved essential for the implementation of screening and endemic for malaria such as Mediterranean countries, prenatal diagnosis programs. In addition, these muta- Africa and Southeast Asia, where carriers of the disease tions can be used as genetic markers to study the origin and spread of β-thalassemia genes, revealing historical relationships between populations. ∗ Corresponding author: Pierre A. Zalloua, Ph.D. Department In Lebanon, β-thalassemia is the most predominant of Obstetrics and Gynecology, American University of Beirut, genetic defect (Hamamy & Alwan, 1994). Being located PO Box: 113-6044, Beirut, Lebanon. Phone: 961-1-350000 ext in the Eastern Mediterranean Basin, Lebanon is a 4805. Fax: 961-1-370829. E-mail: [email protected] crossroads between Europe, Asia and Africa, C University College London 2004 Annals of Human Genetics (2005) 69,55–66 55 NJ.Makhoul et al. allowing settlement and intermingling of succes- 30 (G>C), IVS-I-1 (G>A), IVS-I-6 (T>C), IVS-I- sive different racial groups throughout history. 110 (G>A), cd 44 (−C), IVS-II-1 (G>A), IVS-II-745 Consequently, a melting-pot of seventeen religious (C>G)] were identified using the Amplification Re- groups resides in Lebanon, with over three million fractory Mutation System (ARMS) (Bravo et al. 1999; inhabitants, contributing to its particular heterogeneity. Newton et al. 1989), a PCR technique based on allele- There are two major communities: the Muslim specific priming. The 25 bp deletion and 290 bp dele- community, mainly consisting of Shiites, Sunnis and tion were detected by gap PCR (Faa et al. 1992). The Druze, and the Christian community, mainly consisting βS mutation was studied by PCR amplification followed of Maronites, Greek Orthodox, Greek Catholics by digestion with the restriction enzyme Bsu36I. The and Armenians. Intercommunity marriages are rare, remaining mutations were characterized by direct se- whereas consanguineous marriages exceed 25% in quencing of the amplified DNA using an ABI Prism certain groups (Klat & Khudr, 1986), increasing the 310 genetic analyzer. incidence of affected offspring. Beta thalassemia carrier frequency is estimated to be RFLP Haplotype Analysis between 2% and 3% in Lebanon (Cabannes et al. 1965). β-globin gene RFLP haplotypes were determined us- This frequency is highly variable according to religious ing PCR amplification of fragments containing seven groups, the highest being previously reported for the polymorphic restriction sites around and within the ε- Sunnis, followed closely by the Shiites and then by the Gγ -Aγ -β-δ-β globin gene complex. Following di- Maronites (Zahed et al. 1997). gestion with the specific restriction enzymes (HincII 5 In the present report a total of 520 β-globin chromo- to ε, HindIII within Gγ and Aγ , HincII within and 3 somes from patients with different religious and regional to β, AvaII within β and HinfI 3 to β), samples were backgrounds were studied, reflecting a wide spectrum visualized by ethidium bromide staining after agarose of the population. The aims of this study were to inves- or polyacrylamide gel electrophoresis. RFLP haplotypes tigate the religious and geographic distribution of the were named according to Orkin et al. (1982). β-thalassemia mutations identified in Lebanon, and to trace their precise origins, in the hope of revealing some of the historical relationships that exist between the main Phylogenetic Analysis Lebanese communities and their neighbours. The frequencies of β-thalassemia mutations in Lebanese Materials and Methods samples were used to derive a tree of population relation- ships. The programs GENDIST, SEQBOOT, NEIGH- Subjects BOR and CONSENSE of PHYLIP (Felsenstein, 1993) were used, with 100 bootstraps. Some popula- β β We studied 255 -thalassemia and 5 Sickle Cell/ - tions were dropped from the analysis because of the small thalassemia patients receiving treatment at the Chronic number of chromosomes. Care Center in Lebanon, the country’s only professional β unit for the prevention and treatment of -thalassemia. Results The patients included in the study were unrelated and information about their religious and geographic origin Mutational Analysis was noted. Of the total 520 chromosomes investigated for β-globin gene mutations, only one remained unknown, even af- DNA Preparation and Mutation Screening ter β-globin gene sequence analysis. Twenty different DNA was extracted from peripheral blood leucocytes β-globin mutations were identified, leading to both using salt precipitation (Miller et al. 1988). The most β0 (thalassemia major) and β+ (thalassemia intermedia) frequent β-thalassemia mutations [−88 (C>T), −87 phenotypes. The relative frequencies of mutant chro- (C>G), cd 5 (−CT), cd 8 (−AA), cd 29 (C>T), cd mosomes are listed in Table 1. All mutations have been 56 Annals of Human Genetics (2005) 69,55–66 C University College London 2004 Genetic Heterogeneity of β-thalassemia Table 1 Types and Frequencies of β-Thalassemia Mutations and β-Globin variants in Lebanon Mutation Phenotype Number of Chromosomes Number of homozygotes/heterozygotes Frequency (%) IVS-I-110 (G>A) β+ 178 65/48 34.2 IVS-I-1 (G>A) βo 78 29/20 15.0 IVS-I-6 (T>C) β+ 75 28/19 14.4 cd 29 (C>T) β+ 50 22/6 9.6 IVS-II-1 (G>A) βo 45 17/11 8.6 cd5(−CT) βo 26 9/8 5.0 cd 30 (G>C) βo 14 6/2 2.7 cd8(−AA) βo 13 5/3 2.5 cd 44 (−C) βo 8 3/2 1.5 IVS-II-745 (C>G) β+ 6 3/0 1.1 βs βs 5 0/5 1.0 −87 (C>G) β+ 4 1/2 0.8 IVS-I-5 (G>C) β+ 4 2/0 0.8 −88 (C>T) β+ 3 1/1 0.6 290 bp deletion βo 3 1/1 0.6 25 bp deletion βo 2 1/0 0.4 δβ-thalassemia (Sicilian type) δβo 2 1/0 0.4 cd 8/9 (+G) βo 1 0/1 0.2 cd 36/37 (−T) βo 1 0/1 0.2 cd 39 (C>T) βo 1 0/1 0.2 Unknown 1 0/1 0.2 Total 520 194/132 100 previously reported in Lebanon (Chehab et al. 1987; Most heterogeneous was the Sunni group with 16 Zahed et al. 1997), except for the frameshift at cd 36/37 different mutations. The Mediterranean IVS-I-110 mu- (−T). Six mutations accounted for 87% of the Lebanese tation was the most common, followed by IVS-I-6 and β-thalassemia chromosomes; these were, in decreasing IVS-II-1. Two mutations seemed to be exclusive to order of frequency, IVS-I-110 (G>A), IVS-I-1 (G>A), this group, the Asian Indian IVS-I-5 (G>C) and the IVS-I-6 (T>C), cd 29 (C>T) and cd 5 (−CT). Mediterranean cd 8 (-AA), and these were not found in any other religious group in our study. Religious Distribution of β-Thalassemia Thirteen different β-globin mutations were present Mutations in Shiite subjects. The cd 30 (G>C) mutation was ex- The frequency and distribution of β-thalassemia mu- clusive to the Shiite group and all but two of the cd 29 tations by the various religious groups in Lebanon are mutations were found in this group. presented in Figures 1 and 2.
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