The effects of old and recent migration waves in the distribution of HBB*S globin gene haplotypes

Lindenau, Juliana D.; Wagner, Sandrine C.; Castro, Simone M. de; Hutz, Mara H.

doi:10.1590/1678-4685-GMB-2016-0032

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Special Series of Articles - 60 Years of The Brazilian Society of Genetics • Genet. Mol. Biol. 39 (4) • Oct-Dec 2016 • https://doi.org/10.1590/1678-4685-GMB-2016-0032 copy

The effects of old and recent migration waves in the distribution of HBB*S globin gene haplotypes

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Sickle cell hemoglobin is the result of a mutation at the sixth amino acid position of the beta (β) globin chain. The HBB*S gene is in linkage disequilibrium with five main haplotypes in the β-globin-like gene cluster named according to their ethnic and geographic origins: Bantu (CAR), Benin (BEN), Senegal (SEN), Cameroon (CAM) and Arabian-Indian (ARAB). These haplotypes demonstrated that the sickle cell mutation arose independently at least five times in human history. The distribution of β^S haplotypes among Brazilian populations showed a predominance of the CAR haplotype. American populations were clustered in two groups defined by CAR or BEN haplotype frequencies. This scenario is compatible with historical records about the slave trade in the Americas. When all world populations where the sickle cell gene occurs were analyzed, three clusters were disclosed based on CAR, BEN or ARAB haplotype predominance. These patterns may change in the next decades due to recent migrations waves. Since these haplotypes show different clinical characteristics, these recent migrations events raise the necessity to develop optimized public health programs for sickle cell disease screening and management.

Keywords
β^S globin haplotypes; sickle cell disease; Hemoglobin S; migration

Population	Haplotypes							Reference
Population	N	CAR	BEN	SEN	CAM	ARAB	Atypical	Reference
Belém (PA)	60	66.7	30.0	3.3	–	–	–	*Pante-de-Sousa et al., 1998*Pante-de-Sousa G, Mousinho-Ribeiro RC, dos Santos EJM, Zago MA and Guerreiro JF (1998) Origin of the hemoglobin S gene in a northern Brazilian population: The combined effects of slave trade and internal migrations. Genet Mol Biol 21:365-373.
Belém (PA)	260	66.0	21.8	10.9	1.3	–	–	Cardoso and Guerreiro, 2006Cardoso GL and Guerreiro JF (2006) African gene flow to North Brazil as revealed by HBB*S gene haplotype analysis. Am J Hum Biol 18:93-98.
Ceará (CE)	44	31.8	43.2	2.3	–	–	22.7	*Galiza Neto et al., 2005*Galiza Neto GC, Pitombeira MS, Vieira HF, Vieira MLC and Farias DAB (2005) Analysis of βSglobin gene haplotypes in Ceará, Brazil. J Bras Patol Med Lab 41:315-321.
Ceará (CE)	68	66.2	22.1	–	–	–	11.8	*Silva et al., 2009*Silva LB, Gonçalves RP and Rabenhorst SHB (2009) Analysis of sickle cell anemia haplotypes in Fortaleza reveals the ethnic origins of Ceará state population. J Bras Patol Med Lab 45:115-118.
Rio Grande do Norte (RN)	94	75.5	12.8	–	6.4	–	5.3	*Cabral et al., 2011*Cabral CHK, Serafim ÉSS, de Medeiros WRDB, Fernandes TAAM, Kimura EM, Costa FF, Sonati MF, Rebecchi IMM and de Medeiros TMD (2011) Determination of βS haplotypes in patients with sickle-cell anemia in the state of Rio Grande do Norte, Brazil. Genet Mol Biol 34:421-424.
Pernambuco (PE)	127	81.1	14.2	–	0.8	–	3.9	*Bezerra et al., 2007*Bezerra MAC, Santos MNN, Araújo AS, Gomes YM, Abath FGC and Bandeira MGC (2007) Molecular variations linked to the grouping of β and α-globin genes in neonatal patients with sickle cell disease in the state of Pernambuco, Brazil. Hemoglobin 31:1-6.
Salvador (BA)	72	48.6	51.4	–	–	–	–	*Costa et al., 1984*Costa FF, Arruda VR, Gonçalves MS, Miranda SRP, Carvalho MH, Sonati MF, Saad SOT, Gesteira F, Fernandes D, Nascimento ML, et al. (1984) βS-gene cluster haplotypes in sickle cell anemia patients from two regions of Brazil. Am J Hematol 46:96-97.
Salvador (BA)	160	48.1	45.6	0.6	–	–	5.6	*Gonçalves et al., 2003*Gonçalves MS, Bomfim GC, Maciel E, Cerqueira I, Lyra I, Zanette A, Bomfim G, Adorno EV, Albuquerque AL, Pontes A, et al. (2003) βS-haplotypes in sickle cell anemia patients from Salvador, Bahia, Northeastern Brazil. Braz J Med Biol Res 36:1283-1288.
Salvador (BA)	250	41.6	55.2	0.4	1.2	0.4	1.2	*Adorno et al., 2008*Adorno EV, Zanette A, Lyra I, Seixas MO, Reis MG and Gonçalves MS (2008) Clinical and molecular characteristics of sickle cell anemia in northeast of Brazil. Genet Mol Biol 31:621-625.
Rio de Janeiro (RJ)	148	54.1	44.6	1.4	–	–	–	Fleury, 2007Fleury MK (2007) Haplótipos do cluster da globina beta em pacientes com anemia falciforme no Rio de Janeiro: Aspectos clínicos e laboratoriais. Rev Bras Anál Clín 39:89-93.
São Paulo (SP)	74	64.9	14.9	1.4	–	–	18.9	*Zago et al., 1992*Zago MA, Figueiredo MS and Ogo SH (1992) Bantu βS cluster haplotype predominates among Brazilian blacks. Am J Phys Anthropol 88:295-298.
São Paulo (SP)	148	62.2	33.8	–	–	–	4.1	*Gonçalves et al., 1994*Gonçalves MS, Nechtman JF, Figueiredo MS, Kerbauy J, Arruda VR, Sonati MF, Saad SOT, Costa FF and Stoming TA (1994) Sickle cell disease in a Brazilian population from São Paulo: A study of the βS haplotypes. Hum Hered 44:322-327.
São Paulo (SP)	74	60.8	36.5	–	–	–	2.7	*Costa et al., 1984*Costa FF, Arruda VR, Gonçalves MS, Miranda SRP, Carvalho MH, Sonati MF, Saad SOT, Gesteira F, Fernandes D, Nascimento ML, et al. (1984) βS-gene cluster haplotypes in sickle cell anemia patients from two regions of Brazil. Am J Hematol 46:96-97.
Rio Grande do Sul (RS)	220	67.3	25.0	0.5	0.9	–	6.4	Present study

Continents	Population	N	Haplotypes						Reference
Continents	Population	N	CAR	BEN	SEN	CAM	ARAB	Atypical	Reference
Africa	Algeria	20	–	100.0	–	–	–	–	*Pagnier et al., 1984*Pagnier J, Mears JG, Dunda-Belkhodja O, Schaefer-Rego KE, Beldjord C, Nagel RL and Labie D (1984) Evidence for the multicentric origin of the sickle cell hemoglobin gene in Africa. Proc Natl Acad Sci USA 81:1771-1773.
	Angola	44	95.5	4.5	–	–	–	–	*Lavinha et al., 1992*Lavinha J, Gonçalves J, Faustino P, Romão L, Osório-Almeida L, Peres MJ, Picanço I, Martins MC, Ducrocq R, Labie D, et al. (1992) Importation route of the sickle cell trait into Portugal: Contribution of molecular epidemiology. Hum Biol 64:891-901.
	Cameroon	1082	0.5	73.8	0.2	19.1	0.3	6.1	*Bitoungui et al., 2015*Bitoungui VJN, Pule GD, Hanchard N, Ngogang J andWonkam A (2015) Beta-globin gene haplotypes among Cameroonians and review of the global distribution: Is there a case for a single sickle mutation origin in Africa? OMICS 19:171-179.
	Congo	232	90.9	9.1	–	–	–	–	*Mouélé et al., 1999*Mouélé R, Pambou O, Feingold J and Galactéros F (1999) α-thalassemia in Bantu population from Congo-Brazzaville: Its interaction with sickle cell anemia. Hum Hered 50:118-125.
	Egypt	28	–	100.0	–	–	–	–	*El-Hazmi et al., 1999*El-Hazmi MA, Warsy AS, Bashir N, Beshlawi A, Hussain IR, Temtamy S and Qubaili F (1999) Haplotypes of the ß-globin gene as prognostic factors in sickle-cell disease. East Mediterr Health J 5:1154-1158.
	Guinea	40	22.5	–	–	77.5	–	–	*Sow et al., 1995*Sow A, Peterson E, Josifovska O, Fabry ME, Krishnamoorthy R and Nagel RL (1995) Linkage disequilibrium of the Senegal haplotype with the βS gene in the Republic of Guinea. Am J Hematol 50:301-303.
	Kenya	111	98.2	1.8	–	–	–	–	*Ojwang et al., 1987*Ojwang PJ, Ogada T, Beris P, Hattori Y, Lanclos KD, Kutlar A, Kutlar F and Huisman TH (1987) Haplotypes and a globin gene analyses in sickle cell anaemia patients from Kenya. Br J Haematol 65:211-215.
	Madagascar	35	91.4	–	2.9	–	–	5.7	*Hewitt et al., 1996*Hewitt R, Krause A, Goldman A, Campbell G and Jenkins T (1996) Beta-globin haplotype analysis suggests that a major source of Malagasy ancestry is derived from Bantu-speaking Negroids. Am J Hum Genet 58:1303.
	Mauritania	90	4.4	8.9	77.8	–	5.6	3.3	*Veten et al., 2012*Veten FM, Abdelhamid IO, Meiloud GM, Ghaber SM, Salem ML, Abbes S and Houmeida AO (2012) Hb S [β6 (A3) Glu/Val, GAG > GTG] and β-globin gene cluster haplotype distribution in Mauritania. Hemoglobin 36:311-315.
	Nigeria	669	0.9	93.3	–	3.4	–	2.4	*Adekile et al., 1992*Adekile AD, Kitundu MN, Gu LH, Lanclos KD, Adeodu OO and Huisman TH (1992) Haplotypes in SS patients from Nigeria; characterization of one atypical beta S haplotype no. 19 (Benin) associated with elevated HB F and high G gamma levels. Ann Hematol 65:41-45.
	Senegal	90	–	–	100.0	–	–	–	*Currat et al., 2002*Currat M, Trabuchet G, Rees D, Perrin P, Harding RM, Clegg JB, Langaney A and Excoffier L (2002) Molecular analysis of the β-globin gene cluster in the Niokholo Mandenka population reveals a recent origin of the β-S Senegal mutation. Am J Hum Genet 70:207-223.
	Sudan	143	2.8	29.4	18.2	35.0	–	14.7	*Elderdery et al., 2012*Elderdery AY, Mills J, Mohamed BA, Cooper AJ, Mohammed AO, Eltieb N and Old J (2012) Molecular analysis of the β-globin gene cluster haplotypes in a Sudanese population with sickle cell anemia. Int J Lab Hematol 34:262-266.
	Tanzania	41	100.0	–	–	–	–	–	*Oner et al., 1992*Oner C, Dimovski AJ, Olivieri NF, Schiliro G, Codrington JF, Fattoum S, Adekile AD, Oner R, Yüregir GT, Altay C, et al. (1992) Beta S haplotypes in various world populations. Hum Genet 89:99-104.
	Tunisia	332	2.7	60.5	–	–	–	36.7	*Moumni et al., 2011*Moumni I, Ikbel BMM, Leila C, Fethi M, Amine Z, Mohamed B and Salem A (2011) Restriction mapping of βS locus among Tunisian sickle cell patients. Am J Hum Biol 23:815-819.
	Uganda	208	99.5	–	0.5	–	–	–	*Mpalampa et al., 2012*Mpalampa L, Ndugwa CM, Ddungu H and Idro R (2012) Foetal haemoglobin and disease severity in sickle cell anaemia patients in Kampala, Uganda. BMC Hematol 12:e11.
America	Brazil	1176	65.0	31.5	3.0	0.5	–	–	^* * mean frequency for Brazilian populations showed in Table 1;
	Canada	61	11.5	49.2	13.1	13.1	–	13.1	*Oner et al., 1992*Oner C, Dimovski AJ, Olivieri NF, Schiliro G, Codrington JF, Fattoum S, Adekile AD, Oner R, Yüregir GT, Altay C, et al. (1992) Beta S haplotypes in various world populations. Hum Genet 89:99-104.
	Colombia	229	29.7	33.2	4.4	4.4	0.4	27.9	*Fong et al., 2013*Fong C, Lizarralde-Iragorri MA, Rojas-Gallardo D and Barreto G (2013) Frequency and origin of haplotypes associated with the beta-globin gene cluster in individuals with trait and sickle cell anemia in the Atlantic and Pacific coastal regions of Colombia. Genet Mol Biol 36:494-497.
	Cuba	198	40.9	51.0	8.1	–	–	–	*Muniz et al., 1995*Muniz A, Corral L, Alaez C, Svarch E, Espinosa E, Carbonell N, di Leo R, Felicetti L, Nagel RL and Martinez G(1995) Sickle cell anemia and beta-gene cluster haplotypes in Cuba. Am J Hematol 49:163-164.
	Guadeloupe	830	11.1	74.9	6.1	2.3	0.7	5.1	*Kéclard et al., 1997*Kéclard L, Romana M, Lavocat E, Saint-Martin C, Berchel C and Mérault G(1997) Sickle cell disorder, beta-globin gene cluster haplotypes and alpha-thalassemia in neonates and adults from Guadeloupe. Am J Hematol 55:24-27.
	Jamaica	446	8.3	76.0	5.2	–	–	10.5	*Mpalampa et al., 2012*Mpalampa L, Ndugwa CM, Ddungu H and Idro R (2012) Foetal haemoglobin and disease severity in sickle cell anaemia patients in Kampala, Uganda. BMC Hematol 12:e11.
	Mexico	33	78.8	18.2	–	–	–	3.0	*Magaña et al., 2002*Magaña MT, Ongay Z, Tagle J, Bentura G, Cobián JG, Perea FJ, Casas-Castañeda M, Sánchez-López YJ and Ibarra B (2002) Analysis of beta S and beta A genes in a Mexican population with African roots. Blood Cells Mol Dis 28:121-126.
	Panama	200	51.0	30.0	8.5	4.0	1.0	5.5	*Rusanova et al., 2011*Rusanova I, Cossio G, Moreno B, Javier Perea F, De Borace RG, Perea M, Escames G and Acuña-Castroviejo D (2011) β-globin gene cluster haplotypes in sickle cell patients from Panama. Am J Hum Biol 23:377-380.
	Surinam	77	29.9	53.2	2.6	2.6	–	11.7	*Oner et al., 1992*Oner C, Dimovski AJ, Olivieri NF, Schiliro G, Codrington JF, Fattoum S, Adekile AD, Oner R, Yüregir GT, Altay C, et al. (1992) Beta S haplotypes in various world populations. Hum Genet 89:99-104.
	Trinidad	283	17.3	61.8	8.5	3.5	3.2	5.6	*Jones-Lecointe et al., 2008*Jones-Lecointe A, Smith E, Romana M, Gilbert MG, Charles WP, Saint-Martin C and Kéclard L(2008) Beta-globin gene cluster haplotypes and alpha-thalassemia in sickle cell disease patients from Trinidad. Am J Hum Biol 20:342-344.
	USA	806	16.0	62.4	9.4	4.7	1.5	6.0	*Crawford et al., 2002*Crawford DC, Caggana M, Harris KB, Lorey F, Nash C, Pass KA, Tempelis C and Olney RS (2002) Characterization of β-globin haplotypes using blood spots from a population-based cohort of newborns with homozygous HbS. Genet Med 4:328-335.
	Uruguay	10	60.0	20.0	–	–	–	20.0	*Luz et al., 2006*Luz JÁ, Sans M, Kimura EM, Albuquerque DM, Sonati MF and Costa FF (2006) Alpha-thalassemia, Hb S, and beta-globin gene cluster haplotypes in two Afro- Uruguayan sub-populations from northern and southern Uruguay. Genet Mol Biol 29:595-600.
	Venezuela	359	36.4	51.5	10.6	1.5	–	–	^ mean frequency for Arends et al., 2000; Moreno et al., 2002.
Asia	Bahrain	37	5.4	2.7	–	–	89.2	2.7	Al-Arrayed and Haltes, 1995Al-Arrayed SS and Haltes N (1995) Features of sickle-cell disease in Bahrain. East Mediterr Health J 1:112-118.
	India	140	–	–	–	–	91.4	8.6	*Mukherjee et al., 2004*Mukherjee MB, Surve RR, Gangakhedkar RR, Ghosh K, Colah RB and Mohanty D (2004) Beta-globin gene cluster haplotypes linked to the beta S gene in western India. Hemoglobin 28:157-161.
	Iraq	128	7.8	69.5	–	–	12.5	10.2	*Al-Allawi et al., 2012*Al-Allawi NA, Jalal SD, Nerwey FF, Al-Sayan GO, Al-Zebari SS, Alshingaly AA, Markous RD, Jubrael JM and Hamamy H (2012) Sickle cell disease in the Kurdish population of northern Iraq. Hemoglobin 36:333-342.
	Iran	162	3.1	11.7	3.7	2.5	53.7	25.3	*Rahimi et al., 2003*Rahimi Z, Karimi M, Haghshenass M andMerat A (2003) Beta-globin gene cluster haplotypes in sickle cell patients from southwest Iran. Am J Hematol 74:156-160.
	Jordan	20	–	80.0	–	–	20.0	–	*El-Hazmi et al., 1999*El-Hazmi MA, Warsy AS, Bashir N, Beshlawi A, Hussain IR, Temtamy S and Qubaili F (1999) Haplotypes of the ß-globin gene as prognostic factors in sickle-cell disease. East Mediterr Health J 5:1154-1158.
	Kuwait	125	5.6	11.2	–	–	80.8	2.4	Adekile and Haider, 1996Adekile AD and Haider MZ (1996) Morbidity, βS haplotype and α-globin gene patterns among sickle cell anemia patients in Kuwait. Acta Haematol 96:150-154.
	Lebanon	100	15.0	73.0	–	–	10.0	2.0	*Inati et al., 2003*Inati A, Taher A, Bou Alawi W, Koussa S, Kaspar H, Shbaklo H and Zalloua PA (2003) Beta-globin gene cluster haplotypes and HbF levels are not the only modulators of sickle cell disease in Lebanon. Eur J Haematol 70:79-83.
	Oman	117	21.4	52.1	–	–	26.5	–	*Daar et al., 2000*Daar S, Hussain HM, Gravell D, Nagel RL and Krishnamoorthy R (2000) Genetic epidemiology of Hb S in Oman: Multicentric origin for the beta S gene. Am J Hematol 64:39-46.
	Palestine	118	5.1	88.1	–	–	–	6.8	*Samarah et al., 2009*Samarah F, Ayesh S, Athanasiou M, Christakis J and Vavatsi N (2009) BetaS-globin gene cluster haplotypes in the West Bank of Palestine. Hemoglobin 33:143-149.
	Saudi-Arabia	124	–	98.4	–	–	1.6	–	*El-Hazmi et al., 1999*El-Hazmi MA, Warsy AS, Bashir N, Beshlawi A, Hussain IR, Temtamy S and Qubaili F (1999) Haplotypes of the ß-globin gene as prognostic factors in sickle-cell disease. East Mediterr Health J 5:1154-1158.
	Syria	18	–	66.7	–	–	33.3	–	*El-Hazmi et al., 1999*El-Hazmi MA, Warsy AS, Bashir N, Beshlawi A, Hussain IR, Temtamy S and Qubaili F (1999) Haplotypes of the ß-globin gene as prognostic factors in sickle-cell disease. East Mediterr Health J 5:1154-1158.
	United Arab Emirates	94	25.5	22.3	–	–	52.1	–	El-Kalla and Baysal, 1998El-Kalla S and Baysal E (1998) Genotype-phenotype correlation of sickle cell disease in the United Arab Emirates. J Pediatr Hematol Oncol 15:237-242.
Europe	Greece	14	–	92.9	7.1	–	–	–	*Oner et al., 1992*Oner C, Dimovski AJ, Olivieri NF, Schiliro G, Codrington JF, Fattoum S, Adekile AD, Oner R, Yüregir GT, Altay C, et al. (1992) Beta S haplotypes in various world populations. Hum Genet 89:99-104.
	Italy	64	–	100.0	–	–	–	–	*Schilirò et al., 1992*Schilirò G, Samperi P, Consalvo C, Gangarossa S, Testa R, Miraglia V and Lo Nigro L (1992) Clinical, hematological, and molecular features in Sicilians with sickle cell disease. Hemoglobin 16:469-480.
	Portugal	33	42.4	36.4	21.2	–	–	–	*Lavinha et al., 1992*Lavinha J, Gonçalves J, Faustino P, Romão L, Osório-Almeida L, Peres MJ, Picanço I, Martins MC, Ducrocq R, Labie D, et al. (1992) Importation route of the sickle cell trait into Portugal: Contribution of molecular epidemiology. Hum Biol 64:891-901.
	Turkey	214	–	96.3	–	–	0.5	3.3	*Oner et al., 1992*Oner C, Dimovski AJ, Olivieri NF, Schiliro G, Codrington JF, Fattoum S, Adekile AD, Oner R, Yüregir GT, Altay C, et al. (1992) Beta S haplotypes in various world populations. Hum Genet 89:99-104.

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[1] Send correspondence to Mara H. Hutz. Departamento de Genética, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, 9500, Caixa Postal 15053 91501-970 Porto Alegre, RS, Brazil. E-mail: mara.hutz@ufrgs.br