High prevalence of hepatitis B virus genotype E in Northern Madagascar indicates a West-African lineage

Journal of Medical Virology

Volumn 82, Issue 9, 2010, Pages 1515-1526

  Dupinay, Tatiana ^a,b,c   Restorp, Karin ^d   Leutscher, Peter ^e,f   Rousset, Dominique ^g   Chemin, Isabelle ^a   Migliani, Rene ^e   Magnius, Lars ^d   Norder, Heléne ^d  

^a INSERM   (France)

^b UNIVERSITÉ LYON 1   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^e INSTITUT PASTEUR DE MADAGASCAR   (Madagascar)

^f AARHUS UNIVERSITY HOSPITAL   (Denmark)

^g SERVICE DE SANTÉ DES ARMÉES   (France)

Author keywords

Africa; Genotyping; HBV; Human migration; Molecular epidemiology

Indexed keywords

HEPATITIS B SURFACE ANTIGEN; HEPATITIS E ANTIGEN;

ADOLESCENT; ADULT; AFRICA; ARTICLE; DISEASE MARKER; FEMALE; GENOTYPE; HEPATITIS B; HUMAN; MADAGASCAR; MAJOR CLINICAL STUDY; MALE; MOLECULAR PHYLOGENY; NUCLEOTIDE SEQUENCE; PHYLOGENY; PREVALENCE; SEROPREVALENCE; UNINDEXED SEQUENCE; VIRUS STRAIN;

ADOLESCENT; ADULT; AFRICA, WESTERN; FEMALE; HEPATITIS ANTIBODIES; HEPATITIS B; HEPATITIS B CORE ANTIGENS; HEPATITIS B E ANTIGENS; HEPATITIS B SURFACE ANTIGENS; HEPATITIS B VIRUS; HUMANS; MADAGASCAR; MALE; MIDDLE AGED; MOLECULAR EPIDEMIOLOGY; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROMOTER REGIONS, GENETIC; VIRAL ENVELOPE PROTEINS;

HEPATITIS B VIRUS; SACCHARUM;

EID: 77956596972     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.21865     Document Type: Article

References (76)

1. Abebe A, Nokes DJ, Dejene A, Enquselassie F, Messele T, Cutts FT. 2003. Seroepidemiology of hepatitis B virus in Addis Ababa, Ethiopia: Transmission patterns and vaccine control. Epidemiol Infect 131:757-770.
2. Abiodun PO, Olomu A, Okolo SN, Obasohan A, Freeman O. 1994. The prevalence of hepatitis Be antigen and anti-HBE in adults in Benin City. West Afr J Med 13:171-174.
3. Abou Chekaraow M, Brichler S, Mansour W, LeGal F, Garba A, Deny P, Gordien E. 2010. A novel hepatitis B virus (HBV) subgenotype D (D8) strain, resulting from recombination between ghenotypes D and E, is circulating in Niger along with HBV/E strains. J Gen Virol 91:1609-1620.
4. Arauz-Ruiz P, Norder H, Visona KA, Magnius LO. 1997. Genotype F prevails in HBV infected patients of hispanic origin in Central America and may carry the precore stop mutant. J Med Virol 51:305-312.
5. Arauz-Ruiz P, Norder H, Robertson BH, Magnius LO. 2002. Genotype H: A new Amerindian genotype of hepatitis B virus revealed in Central America. J Gen Virol 83:2059-2073.
6. Banerjee A, Kurbanov F, Datta S, Chandra PK, Tanaka Y, Mizokami M, Chakravarty R. 2006. Phylogenetic relatedness and genetic diversity of hepatitis B virus isolates in Eastern India. J Med Virol 78:1164-1174.
7. Boisier P, Rabarijaona L, Piollet M, Roux JF, Zeller HG. 1996. Hepatitis Bvirus infection in general population in Madagascar: Evidence for different epidemiological patterns in urban and in rural areas. Epidemiol Infect 117:133-137.
8. Bowyer SM, van Staden L, Kew MC, Sim JG. 1997. A unique segment of the hepatitis B virus group A genotype identified in isolates from South Africa. J Gen Virol 78:1719-1729.
9. Brunetto MR, Giarin M, Saracco G, Oliveri F, Calvo P, Capra G, Randone A, Abate ML, Manzini P, Capalbo M. 1993. Hepatitis B virus unable to secrete e antigen and response to interferon in chronic hepatitis B. Gastroenterology 105:845-850.
10. Cavinta L, Sun J, May A, Yin J, von Meltzer M, Radtke M, Barzaga NG, Cao G, Schaefer S. 2009. A new isolate of hepatitis B virus from the Philippines possibly representing a new subgenotype C6. J Med Virol 81:983-987.
11. Chandra PK, Biswas A, Datta S, Banerjee A, Panigrahim R, Chakrabarti S, De BK, Chakravarty R. 2009. Subgenotypes of hepatitis B virus genotype D (D1, D2, D3 and D5) in India: Differential pattern of mutations, liver injury and occult HBV infection. J Viral Hepat 16:749-756.
12. Chow RA, Caeiro JL, Chen SJ, Garcia-Bertrand RL, Herrera RJ. 2005. Genetic characterization of four Austronesian-speaking populations. J Hum Genet 50:550-559.
13. Chu CM, Yeh CT, Lee CS, Sheen IS, Liaw YF. 2002. Precore stop mutant in HBeAg-positive patients with chronic hepatitis B: Clinical characteristics and correlation with the course of HBeAg-to-anti-HBe seroconversion. J Clin Microbiol 40:16-21.
14. Dahl OC. 1988. Bantu substratum in Malagasy. Etudes Océan Indien 9:91-132.
15. Devesa M, Loureiro CL, Rivas Y, Monsalve F, Cardona N, Duarte MC, Poblete F, Gutierrez MF, Botto C, Pujol FH. 2008. Subgenotype diversity of hepatitis B virus American genotype F in Amerindians from Venezuela and the general population of Colombia. J Med Virol 80:20-26.
16. Felstenstein J. 1993. PHYLIP: Phylogeni inference package, Version3.52c. Seattle, WA: University of Washington.
17. Fujiwara K, Tanaka Y, Orito E, Ohno T, Kato T, Sugihara K, Hasegawa I, Sakurai M, Ito K, Ozasa A, Sakamoto Y, Arita I, El-Gohary A, Benoit A, Ogoundele-Akplogan SI, Yoshihara N, Ueda R, Mizokami M. 2005. Distribution of HBV genotypes among HBV carriers in Benin:phylogenetic analysis and virological characteristics of HBV genotype E. World J Gastroenterol 11:6410-6415.
18. Ganem D, Varmus HE. 1987. The molecular biology of the hepatitis B viruses. Annu Rev Biochem 56:651-693.
19. Hannoun C, Soderstrom A, Norkrans G, Lindh M. 2005. Phylogeny of African complete genomes reveals a West African genotype A subtype of hepatitis B virus and relatedness between Somali and Asian A1 sequences. J Gen Virol 86:2163-2167.
20. Hannoun C, Norder H, Lindh M. 2000. An abberant genotype revealed in recombinant hepatitis B virus strains from Vietnam. J Gen Virol 81:2267-2272.
21. Hewitt R, Krause A, Goldman A, Campbell G, Jenkins T. 1996. Beta-globin haplotype analysis suggests that amajor source of Malagasy ancestry is derived from Bantu-speaking Negroids. Am J Hum Genet 58:1303-1308.
22. Hurles ME, Sykes BC, Jobling MA, Forster P. 2005. The dual origin of the Malagasy in Island Southeast Asia and East Africa: Evidence from maternal and paternal lineages. Am J Hum Genet 76:894-901.
23. Kao JH. 2002. Hepatitis B viral genotype: Clinical relevance and molecular characteristics. J Gastroenterol Hepatol 17:643-650.
24. Kramvis A, Kew MC. 2007. Molecular characterization of subgenotype A1 (subgroup Aa) of hepatitis B virus. Hepatol Res 37:S27-S32.
25. Kramvis A, Bukofzer S, Kew MC, Song E. 1997. Nucleic acid sequence analysis of the precore region of hepatitis B virus from sera of southern African black adult carriers of the virus. Hepatology 25:235-240.
26. Kramvis A, Weitzmann L, Owiredu WK, Kew MC. 2002. Analysis of the complete genome of subgroup A′ hepatitis B virus isolates from South Africa. J Gen Virol 83:835-839.
27. Kramvis A, Restorp K, Norder H, Botha JF, Magnius LO, Kew MC. 2005. Full genome analysis of hepatitis B virus genotype E strains from South-Western Africa and Madagascar reveals low genetic variability. J Med Virol 77:47-52.
28. Kumagai I, Abe K, Oikawa T, Sato A, Sato S, Endo R, Takikawa Y, Suzuki K, Masuda T, Sainokami S, Endo K, Takahashi M, Okamoto H. 2007. A male patient with severe acute hepatitis who was domestically infected with a genotype H hepatitis B virus in Iwate. Jpn J Gastroenterol 42:168-175.
29. Kurbanov F, Tanaka Y, Fujiwara K, Sugauchi F, Mbanya D, Zekeng L, Ndembi N, Ngansop C, Kaptue L, Miura T, Ido E, Hayami M, Ichimura H, Mizokami M. 2005. A new subtype (subgenotype) Ac (A3) of hepatitis B virus and recombination between genotypes A and E in Cameroon. J Gen Virol 86:2047-2056.
30. Leutscher PD, Ramarokoto CE, Hoffmann S, Jensen JS, Ramaniraka V, Randrianasolo B, Raharisolo C, Migliani R, Christensen N. 2008. Coexistence of urogenital schistosomiasis and sexually transmitted infection in women and men living in an area where Schistosoma haematobium is endemic. Clin Infect Dis 47:775-782.
31. Lok AS, Akarca U, Greene S. 1994. Mutations in the pre-core region of hepatitis B virus serve to enhance the stability of the secondary structure of the pre-genome encapsidation signal. Proc Natl Acad Sci USA 91:4077-4081.
32. Lusida MI, Nugrahaputra VE, Soetjipto Handajani R, Nagano-Fujii M, Sasayama M, Utsumi T, Hotta H. 2008. Novel subgenotypes of hepatitis B virus genotypes C and D in Papua, Indonesia. J Clin Microbiol 46:2160-2166.
33. Mafrezi A, Randretsa I. 1985. Evolution and structure of the population of Madagascar. Demogr Afr 48-49:51-60.
34. Makuwa M, Souquiere S, Telfer P, Apetrei C, Vray M, Bedjabaga I, Mouinga-Ondeme A, Onanga R, Marx PA, Kazanji M, Roques P, Simon F. 2006. Identification of hepatitis B virus subgenotype A3 in rural Gabon. J Med Virol 78:1175-1184.
35. Markov PV, Pepin J, Frost E, Deslandes S, Labbe AC, Pybus OG. 2009. Phylogeography and molecular epidemiology of hepatitis C virus genotype 2 in Africa. J Gen Virol 90:2086-2096.
36. McMahon BJ. 2009. The influence of hepatitis B virus genotype and subgenotype on the natural history of chronic hepatitis B. Hepatol Int 3:334-342.
37. Meldal BH, Moula NM, Barnes IH, Boukef K, Allain JP. 2009. A novel hepatitis B virus subgenotype, D7, in Tunisian blood donors. J Gen Virol 90:1622-1628.
38. Migliani R, Rakoto Andrianarivelo M, Rousset D, Rabarijaona L, Randrianarisoa P, Roux JF. 2000a. Seroprevalence of viral hepatitis B in the city of Mahajanga, Madagascar in 1999. Med Trop (Mars) 60:146-150.
39. Migliani R, Rousset D, Rakoto-Andrianarivelo M, Rabarijaona L, Ratsitorahina M, Rajaonarivony V, Mauclere P. 2000b. Hepatitis B virus infection: A public health problem in Madagascar. Arch Inst Pasteur Madagascar 66:50-54.
40. Migot F, Perichon B, Danze PM, Raharimalala L, Lepers JP, Deloron P, Krishnamoorthy R. 1995. HLA class II haplotype studies bring molecular evidence for population affinity between Madagascans and Javanese. Tissue Antigens 46:131-135.
41. Morvan JM, Boisier P, Andrianimanana D, Razainirina J, Rakoto-Andrianarivelo M, Roux JF. 1994. Serological markers for hepatitis A, B and C in Madagascar. First investigation in a rural area. Bull Soc Pathol Exot 87:138-142.
42. Mulders MN, Venard V, Njayou M, Edorh AP, Bola Oyefolu AO, Kehinde MO, Muyembe Tamfum JJ, Nebie YK, Maiga I, Ammerlaan W, Fack F, Omilabu SA, Le Faou A, Muller CP. 2004. Low genetic diversity despite hyperendemicity of hepatitis B virus genotype E throughout West Africa. J Infect Dis 190:400-408.
43. Mulyanto Depamede SN, Surayah K, Tsuda F, Ichiyama K, Takahashi M, Okamoto H. 2009. A nationwide molecular epidemiological study on hepatitis B virus in Indonesia: Identification of two novel subgenotypes, B8 and C7. Arch Virol 154:1047-1059.
44. Nagasaki F, Niitsuma H, Cervantes JG, Chiba M, Hong S, Ojima T, Ueno Y, Bondoc E, Kobayashi K, Ishii M, Shimosegawa T. 2006. Analysis of the entire nucleotide sequence of hepatitis B virus genotype B in the Philippines reveals a new subgenotype of genotype B. J Gen Virol 87:1175-1180.
45. Naumann H, Schaefer S, Yoshida CF, Gaspar AM, Repp R, Gerlich WH. 1993. Identification of a new hepatitis B virus (HBV) genotype from Brazil that expresses HBV surface antigen subtype adw4. J Gen Virol 74:1627-1632.
46. Norder H, Courouce AM, Magnius LO. 1992. Molecular basis of hepatitis B virus serotype variations within the four major subtypes. J Gen Virol 73:3141-3145.
47. Norder H, Courouce AM, Magnius LO. 1994. Complete genomes, phylogenetic relatedness, and structural proteins of six strains of the hepatitis B virus, four of which represent two new genotypes. Virology 198:489-503.
48. Norder H, Courouce AM, Coursaget P, Echevarria JM, Lee SD, Mushahwar IK, Robertson BH, Locarnini S, Magnius LO. 2004. Genetic diversity of hepatitis B virus strains derived worldwide: Genotypes, subgenotypes, and HBsAg subtypes. Intervirology 47:289-309.
49. Nurainy N, Muljono DH, Sudoyo H, Marzuki S. 2008. Genetic study of hepatitis B virus in Indonesia reveals a new subgenotype of genotype B in east Nusa Tenggara. Arch Virol 153:1057-1065.
50. Odemuyiwa SO, Mulders MN, Oyedele OI, Ola SO, Odaibo GN, Olaleye DO, Muller CP. 2001. Phylogenetic analysis of new hepatitis B virus isolates from Nigeria supports endemicity of genotype E in West Africa. J Med Virol 65:463-469.
51. Okamoto H, Imai M, Tsuda F, Tanaka T, Miyakawa Y, Mayumi M. 1987. Point mutation in the S gene of hepatitis B virus for a d/y or w/r subtypic change in two blood donors carrying a surface antigen of compound subtype adyr or adwr. J Virol 61:3030-3034.
52. Olinger CM, Venard V, Njayou M, Oyefolu AO, Maiga I, Kemp AJ, Omilabu SA, le Faou A, Muller CP. 2006. Phylogenetic analysis of the precore/core gene of hepatitis B virus genotypes E and A in West Africa: New subtypes, mixed infections and recombinations. J Gen Virol 87:1163-1173.
53. Orito E, Mizokami M, Sakugawa H, Michitaka K, Ishikawa K, Ichida T, Okanoue T, Yotsuyanagi H, Iino S. 2001. A case-control study for clinical and molecular biological differences between hepatitis B viruses of genotypes B and C. Hepatology 33:218-223.
54. Pawlotsky JM, Belec L, Gresenguet G, Deforges L, Bouvier M, Duval J, Dhumeaux D. 1995. High prevalence of hepatitis B, C, and E markers in young sexually active adults from the Central African Republic. J Med Virol 46:269-272.
55. Pourkarim MR, Lemey P, Amini-Bavil-Olyaee S, Maes P, Van Ranst M. 2010. Novel hepatitis B virus subgenotype A6 in African-Belgian patients. J Clin Virol 47:93-106.
56. Quintero A, Martinez D, Alarcon De Noya B, Costagliola A, Urbina L, Gonzalez N, Liprandi F, Castro De Guerra D, Pujol FH. 2002. Molecular epidemiology of hepatitis B virus in Afro-Venezuelan populations. Arch Virol 147:1829-1836.
57. Ramarakoto CE, Leutscher PD, van Dam G, Christensen NO. 2008. Ultrasonographical findings in the urogenital organs in women and men infected with Schistosoma haematobium in northern Madagascar. Trans R Soc Trop Med Hyg 102:767-773.
58. Rapicetta M, Stroffolini T, Ngatchu T, Chionne P, Ciccaglione AR, Lantum D, Chiaramonte M. 1991. Age- and sex-related study of HBV-DNA in HBsAg asymptomatic children from an endemic area (Cameroon). Ann Trop Paediatr 11:325-329.
59. Regueiro M, Mirabal S, Lacau H, Caeiro JL, Garcia-Bertrand RL, Herrera RJ. 2008. Austronesian genetic signature in East African Madagascar and Polynesia. J Hum Genet 53:106-120.
60. Sakamoto T, Tanaka Y, Orito E, Co J, Clavio J, Sugauchi F, Ito K, Ozasa A, Quino A, Ueda R, Sollano J, Mizokami M. 2006. Novel subtypes (subgenotypes) of hepatitis B virus genotypes B and C among chronic liver disease patients in the Philippines. J Gen Virol 87:1873-1882.
61. Sanchez LV, Tanaka Y, Maldonado M, Mizokami M, Panduro A. 2007. Difference of hepatitis B virus genotype distribution in two groups of mexican patients with different risk factors. High prevalence of genotype H and G. Intervirology 50:9-15.
62. Schaefer S. 2007. Hepatitis B virus taxonomy and hepatitis B virus genotypes. World J Gastroenterol 13:14-21.
63. Schaefer S, Magnius L, Norder H. 2009. Under construction: Classification of hepatitis B virus genotypes and subgenotypes. Intervirology 52:323-325.
64. Sendi H, Mehrab-Mohseni M, Zali MR, Norder H, Magnius LO. 2005. T1764G1766 core promoter double mutants are restricted to hepatitis B virus strains with an A1757 and are common in genotype D. J Gen Virol 86:2451-2458.
65. Singer R, Budtz-Olsen OE, Brain P, Saugrain J. 1957. Physical features, sickling and serology of the Malagasy of Madagascar. Am J Phys Anthropol 15:91-124.
66. Singh J, Dickens C, Pahal V, Kumar R, Chaudhary R, Kramvis A, Kews MC. 2009. First report of genotype e of hepatitis B virus in an Indian population. Intervirology 52:235-238.
67. Soodyall H, Jenkins T, Stoneking M. 1995. 'Polynesian' mtDNA in the Malagasy. Nat Genet 10:377-378.
68. Stuyver L, De Gendt S, Van Geyt C, Zoulim F, Fried M, Schinazi RF, Rossau R. 2000. A new genotype of hepatitis B virus: Complete genome and phylogenetic relatedness. J Gen Virol 81:67-74.
69. Sugauchi F, Kumada H, Acharya SA, Shrestha SM, Gamutan MT, Khan M, Gish RG, Tanaka Y, Kato T, Orito E, Ueda R, Miyakawa Y, Mizokami M. 2004. Epidemiological and sequence differences between two subtypes (Ae and Aa) of hepatitis B virus genotype A. J Gen Virol 85:811-820.
70. Suzuki S, Sugauchi F, Orito E, Kato H, Usuda S, Siransy L, Arita L, Sakamoto Y, Yoshihara N, El-Gohary A, Ueda R, Mizokami M. 2003. Distribution of hepatitis B virus (HBV) genotypes among HBV carriers in the Cote d'Ivoire: Complete genome sequence and phylogenetic relatedness of HBV genotype E. J Med Virol 69:459-465.
71. Tallo T, Tefanova V, Priimägi L, Schmidt J, Katargina O, Michailov M, Mukomolov S, Magnius L, Norder H. 2008. D2: Major subgenotype of hepatitis B virus in Russia and the Baltic region. J Gen Virol 89:1829-1839.
72. Tanaka Y, Hasegawa I, Kato T, Orito E, Hirashima N, Acharya SK, Gish RG, Kramvis A, Kew MC, Yoshihara N, Shrestha SM, Khan M, Miyakawa Y, Mizokami M. 2004. A case-control study for differences among hepatitis B virus infections of genotypes A (subtypes Aa and Ae) and D. Hepatology 40:747-755. (Pubitemid 39265598)
73. Tatematsu K, Tanaka Y, Kurbanov F, Sugaucho F, Mano S, Maeshiro T, Nakayoshi T, Wakuta M, Miyakawa Y, Mizonami M. 2009. A genetic variant of hepatitis B virus divergent from known human and ape genotypes isolated from a Japanese patient and provisionally assigned to a new genotype J. J Virol 83:10538-10547.
74. Tran TT, Trinh TN, Abe K. 2008. New complex recombinant genotype of hepatitis B virus identified in Vietnam. J Virol 82:5657-5663.
75. Tswana S, Chetsanga C, Nyström L, Moyo S, Nzara M, Chieza LA. 1996. Sero-epidemiological cross-sectional study of hepatitis B virus in Zimbabwe. S Afr Med J 86:72-75. WHO Hepatitis B. Fact sheet No 204.
76. Wang HY, Li D, Liu W, Jin X, Du B, Li YP, Gu HX, Zhang SY. 2009. Hepatitis B virus subgenotype C2 is the most prevalent subgenotype in northeast China. Clin Microbiol Infect 16:477-481.