1887

Abstract

Niger is a west African country that is highly endemic for hepatitis B virus (HBV) infection. The seroprevalence for HBV surface antigen (HBsAg) is about 20 %; however, there are no reports on the molecular epidemiology of HBV strains spreading in Niger. In the present study, HBV isolates from the sera of 58 consecutive, asymptomatic, HBsAg-positive blood donors were characterized. Genotype affiliation was determined by amplification, sequencing and phylogenetic analysis of the preS1, polymerase/reverse transcriptase (RT/Pol) and precore (preC)/C regions. The first series of results revealed that different genomic fragments clustered with different genotypes on phylogenetic trees, suggesting recombination events. Twenty-four complete genomic sequences were obtained by amplification and sequencing of seven overlapping regions covering the whole genome, and were studied by extensive phylogenetic analysis. Among them, 20 (83.3 %) were classified unequivocally as genotype E (HBV/E). The remaining four (16.7%) clustered on a distinct branch within HBV/D with strong bootstrap and posterior probability values. Complete molecular characterization of these four strains was achieved by the Simplot program, bootscanning analysis and cloning experiments, and enabled us to identify an HBV/D–E recombinant that formed a new HBV/D subgenotype spreading in Niger, tentatively named D8. Moreover, 20 new complete HBV/E nucleotide sequences were determined that exhibited higher genetic variability than is generally described in Africa. One was found to be a recombinant containing HBV/D sequences in the preS2 and RT/Pol regions. Taken together, these data suggest that, in Niger, genetic variability of HBV strains is still evolving, probably reflecting ancient endemic HBV infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.018127-0
2010-06-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/6/1609.html?itemId=/content/journal/jgv/10.1099/vir.0.018127-0&mimeType=html&fmt=ahah

References

  1. Altekar, G., Dwarkadas, S., Huelsenbeck, J. P. & Ronquist, F.(2004). Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20, 407–415.[CrossRef] [Google Scholar]
  2. Andernach, I. E., Hübschen, J. M. & Muller, C. P.(2009). Hepatitis B virus: the genotype E puzzle. Rev Med Virol 19, 231–240.[CrossRef] [Google Scholar]
  3. Arauz-Ruiz, P., Norder, H., Robertson, B. H. & Magnius, L. O.(2002). Genotype H: a new Amerindian genotype of hepatitis B virus revealed in Central America. J Gen Virol 83, 2059–2073. [Google Scholar]
  4. Ayed, K., Gorgi, Y., Ayed-Jendoubi, S., Aouadi, H., Sfar, I., Najjar, T. & Ben Abdallah, T.(2007). Hepatitis B virus genotypes and precore/core-promoter mutations in Tunisian patients with chronic hepatitis B virus infection. J Infect 54, 291–297.[CrossRef] [Google Scholar]
  5. Bahri, O, Cheikh, I., Hajji, N., Djebbi, A., Maamouri, N., Sadraoui, A., Mami, N. B. & Triki, H.(2006). Hepatitis B genotypes, precore and core promoter mutants circulating in Tunisia. J Med Virol 78, 353–357.[CrossRef] [Google Scholar]
  6. Bekondi, C., Olinger, C. M., Boua, N., Talarmin, A., Muller, C. P., Le Faou, A. & Venard, V.(2007). Central African Republic is part of the West-African hepatitis B virus genotype E crescent. J Clin Virol 40, 31–37.[CrossRef] [Google Scholar]
  7. Bollyky, P. L., Rambaut, A., Harvey, P. H. & Holmes, E. C.(1996). Recombination between sequences of hepatitis B virus from different genotypes. J Mol Evol 42, 97–102.[CrossRef] [Google Scholar]
  8. Cavinta, L., Sun, J., May, A., Yin, J., von Meltzer, M., Radtke, M., Barzaga, N. G., 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.[CrossRef] [Google Scholar]
  9. Cenac, A., Pedroso, M. L., Djibo, A., Develoux, M., Pichoud, C., Lamothe, F., Trepo, C. & Warter, A.(1995). Hepatitis B, C, and D virus infections in patients with chronic hepatitis, cirrhosis, and hepatocellular carcinoma: a comparative study in Niger. Am J Trop Med Hyg 52, 293–296. [Google Scholar]
  10. Cui, C., Shi, J., Hui, L., Xi, H., Zhuoma, Quni, Tsedan & Hu, G.(2002). The dominant hepatitis B virus genotype identified in Tibet is a C/D hybrid. J Gen Virol 83, 2773–2777. [Google Scholar]
  11. Dejean, A., Sonigo, P., Wain-Hobson, S. & Tiollais, P.(1984). Specific hepatitis B virus integration in hepatocellular carcinoma DNA through a viral 11-base-pair direct repeat. Proc Natl Acad Sci U S A 81, 5350–5354.[CrossRef] [Google Scholar]
  12. Ezzikouri, S., Chemin, I., Chafik, A., Wakrim, L., Nourlil, J., Malki, A. E., Marchio, A., Dejean, A., Hassar, M. & other authors(2008). Genotype determination in Moroccan hepatitis B chronic carriers. Infect Genet Evol 8, 306–312.[CrossRef] [Google Scholar]
  13. Ganem, D. & Prince, A. M.(2004). Hepatitis B virus infection – natural history and clinical consequences. N Engl J Med 350, 1118–1129.[CrossRef] [Google Scholar]
  14. Ganne-Carrié, N., Williams, V., Kaddouri, H., Trinchet, J. C., Dziri-Mendil, S., Alloui, C., Hawajri, N. A., Dény, P., Beaugrand, M. & Gordien, E.(2006). Significance of hepatitis B virus genotypes A to E in a cohort of patients with chronic hepatitis B in the Seine Saint Denis District of Paris (France). J Med Virol 78, 335–340.[CrossRef] [Google Scholar]
  15. Garmiri, P., Loua, A., Haba, N., Candotti, D. & Allain, J. P.(2009). Deletions and recombinations in the core region of hepatitis B virus genotype E strains from asymptomatic blood donors in Guinea, west Africa. J Gen Virol 90, 2442–2451.[CrossRef] [Google Scholar]
  16. Gunther, S., Li, B. C., Miska, S., Kruger, D. H., Meisel, H. & Will, H.(1995). A novel method for efficient amplification of whole hepatitis B virus genomes permits rapid functional analysis and reveals deletion mutants in immunosuppressed patients. J Virol 69, 5437–5444. [Google Scholar]
  17. Hannoun, C., Norder, H. & Lindh, M.(2000). An aberrant genotype revealed in recombinant hepatitis B virus strains from Vietnam. J Gen Virol 81, 2267–2272. [Google Scholar]
  18. Hino, O., Tabata, S. & Hotta, Y.(1991). Evidence for increased in vitro recombination with insertion of human hepatitis B virus DNA. Proc Natl Acad Sci U S A 88, 9248–9252.[CrossRef] [Google Scholar]
  19. Hubschen, J. M., Andernach, I. E. & Muller, C. P.(2008). Hepatitis B virus genotype E variability in Africa. J Clin Virol 43, 376–380.[CrossRef] [Google Scholar]
  20. Hubschen, J. M., Mugabo, J., Peltier, C. A., Karasi, J. C., Sausy, A., Kirpach, P., Arendt, V. & Muller, C. P.(2009). Exceptional genetic variability of hepatitis B virus indicates that Rwanda is east of an emerging African genotype E/A1 divide. J Med Virol 81, 435–440.[CrossRef] [Google Scholar]
  21. Huelsenbeck, J. P. & Ronquist, F.(2001).mrbayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.[CrossRef] [Google Scholar]
  22. Khelifa, F. & Thibault, V.(2009). Characteristics of hepatitis B viral strains in chronic carrier patients from north-east Algeria. Pathol Biol (Paris) 57, 107–113 (in French).[CrossRef] [Google Scholar]
  23. Kramvis, A. & Kew, M. C.(2007). Epidemiology of hepatitis B virus in Africa, its genotypes and clinical associations of genotypes. Hepatol Res 37, S9–S19.[CrossRef] [Google Scholar]
  24. Kramvis, A., Weitzmann, L., Owiredu, W. K. & Kew, M. C.(2002). Analysis of the complete genome of subgroup A′ hepatitis B virus isolates from South Africa. J Gen Virol 83, 835–839. [Google Scholar]
  25. Kramvis, A., Arakawa, K., Yu, M. C., Nogueira, R., Stram, D. O. & Kew, M. C.(2008). Relationship of serological subtype, basic core promoter and precore mutations to genotypes/subgenotypes of hepatitis B virus. J Med Virol 80, 27–46.[CrossRef] [Google Scholar]
  26. Kurbanov, F.(2008). When should “I” consider a new hepatitis B virus genotype? J Virol 82, 8241–8242.[CrossRef] [Google Scholar]
  27. Kurbanov, F., Tanaka, Y., Fujiwara, K., Sugauchi, F., Mbanya, D., Zekeng, L., Ndembi, N., Ngansop, C., Kaptue, L. & other authors(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.[CrossRef] [Google Scholar]
  28. Laoi, B. N. & Crowley, B.(2008). Molecular characterization of hepatitis B virus (HBV) isolates, including identification of a novel recombinant, in patients with acute HBV infection attending an Irish hospital. J Med Virol 80, 1554–1564.[CrossRef] [Google Scholar]
  29. Lee, D. S., Huh, K., Lee, E. H., Lee, D. H., Hong, K. S. & Sung, Y. C.(1997). HCV and HBV coexist in HBsAg-negative patients with HCV viraemia: possibility of coinfection in these patients must be considered in HBV-high endemic area. J Gastroenterol Hepatol 12, 855–861.[CrossRef] [Google Scholar]
  30. Lok, A. S.(2004). Prevention of hepatitis B virus-related hepatocellular carcinoma. Gastroenterology 127, S303–S309.[CrossRef] [Google Scholar]
  31. Lole, K. S., Bollinger, R. C., Paranjape, R. S., Gadkari, D., Kulkarni, S. S., Novak, N. G., Ingersoll, R., Sheppard, H. W. & Ray, S. C.(1999). Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73, 152–160. [Google Scholar]
  32. Lusida, M. I., Nugrahaputra, V. E., 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.[CrossRef] [Google Scholar]
  33. Mamadou, S., Laouel Kader, A., Rabiou, S., Aboubacar, A., Soumana, O., Garba, A., Delaporte, E. & Mboup, S.(2006). Prevalence of the HIV infection and five other sexually-transmitted infections among sex workers in Niamey, Niger. Bull Soc Pathol Exot 99, 19–22 (in French).[CrossRef] [Google Scholar]
  34. Meldal, B. H., Moula, N. M., Barnes, I. H., Boukef, K. & Allain, J. P.(2009). A novel hepatitis B virus subgenotype, D7, in Tunisian blood donors. J Gen Virol 90, 1622–1628.[CrossRef] [Google Scholar]
  35. Morozov, V., Pisareva, M. & Groudinin, M.(2000). Homologous recombination between different genotypes of hepatitis B virus. Gene 260, 55–65.[CrossRef] [Google Scholar]
  36. Mulders, M. N., Venard, V., Njayou, M., Edorh, A. P., Bola Oyefolu, A. O., Kehinde, M. O., Muyembe Tamfum, J. J., Nebie, Y. K., Maiga, I. & other authors(2004). Low genetic diversity despite hyperendemicity of hepatitis B virus genotype E throughout West Africa. J Infect Dis 190, 400–408.[CrossRef] [Google Scholar]
  37. Mulyanto, Depamede, S. N., 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.[CrossRef] [Google Scholar]
  38. Nagaya, T., Nakamura, T., Tokino, T., Tsurimoto, T., Imai, M., Mayumi, T., Kamino, K., Yamamura, K. & Matsubara, K.(1987). The mode of hepatitis B virus DNA integration in chromosomes of human hepatocellular carcinoma. Genes Dev 1, 773–782.[CrossRef] [Google Scholar]
  39. Norder, H., Courouce, A. M. & Magnius, L. O.(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.[CrossRef] [Google Scholar]
  40. Norder, H., Courouce, A. M., Coursaget, P., Echevarria, J. M., Lee, S. D., Mushahwar, I. K., Robertson, B. H., Locarnini, S. & Magnius, L. O.(2004). Genetic diversity of hepatitis B virus strains derived worldwide: genotypes, subgenotypes, and HBsAg subtypes. Intervirology 47, 289–309.[CrossRef] [Google Scholar]
  41. Nurainy, N., Muljono, D. H., 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.[CrossRef] [Google Scholar]
  42. Okamoto, H., Tsuda, F., Sakugawa, H., Sastrosoewignjo, R. I., Imai, M., Miyakawa, Y. & Mayumi, M.(1988). Typing hepatitis B virus by homology in nucleotide sequence: comparison of surface antigen subtypes. J Gen Virol 69, 2575–2583.[CrossRef] [Google Scholar]
  43. Olinger, C. M., Venard, V., Njayou, M., Oyefolu, A. O., Maiga, I., Kemp, A. J., Omilabu, S. A., le Faou, A. & Muller, C. P.(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.[CrossRef] [Google Scholar]
  44. Olinger, C. M., Lazouskaya, N. V., Eremin, V. F. & Muller, C. P.(2008a). Multiple genotypes and subtypes of hepatitis B and C viruses in Belarus: similarities with Russia and western European influences. Clin Microbiol Infect 14, 575–581.[CrossRef] [Google Scholar]
  45. Olinger, C. M., Jutavijittum, P., Hübschen, J. M., Yousukh, A., Samountry, B., Thammavong, T., Toriyama, K. & Muller, C. P.(2008b). Possible new hepatitis B virus genotype, Southeast Asia. Emerg Infect Dis 14, 1777–1780.[CrossRef] [Google Scholar]
  46. Owiredu, W. K., Kramvis, A. & Kew, M. C.(2001). Hepatitis B virus DNA in serum of healthy black African adults positive for hepatitis B surface antibody alone: possible association with recombination between genotypes A and D. J Med Virol 64, 441–454.[CrossRef] [Google Scholar]
  47. Pineau, P., Marchio, A., Mattei, M.-G., Kim, W.-H., Youn, J.-K., Tiollais, P. & Dejean, A.(1998). Extensive analysis of duplicated-inverted hepatitis B virus integrations in human hepatocellular carcinoma. J Gen Virol 79, 591–600. [Google Scholar]
  48. Schaefer, S.(2007). Hepatitis B virus taxonomy and hepatitis B virus genotypes. World J Gastroenterol 13, 14–21.[CrossRef] [Google Scholar]
  49. Simmonds, P. & Midgley, S.(2005). Recombination in the genesis and evolution of hepatitis B virus genotypes. J Virol 79, 15467–15476.[CrossRef] [Google Scholar]
  50. Soubiran, G., Le Bras, M., Marini, P. & Sekou, H.(1987). High HBsAg and anti-delta carrier rate among asymptomatic Africans living on the campus of the University of Niamey, Niger. Trans R Soc Trop Med Hyg 81, 998–1000.[CrossRef] [Google Scholar]
  51. Stuyver, L., De Gendt, S., Van Geyt, C., Zoulim, F., Fried, M., Schinazi, R. F. & Rossau, R.(2000). A new genotype of hepatitis B virus: complete genome and phylogenetic relatedness. J Gen Virol 81, 67–74. [Google Scholar]
  52. Tatematsu, K., Tanaka, Y., Kurbanov, F., Sugauchi, F., Mano, S., Maeshiro, T., Nakayoshi, T., Wakuta, M., Miyakawa, Y. & Mizokami, 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 new genotype J. J Virol 83, 10538–10547.[CrossRef] [Google Scholar]
  53. Tokino, T., Fukushige, S., Nakamura, T., Nagaya, T., Murotsu, T., Shiga, K., Aoki, N. & Matsubara, K.(1987). Chromosomal translocation and inverted duplication associated with integrated hepatitis B virus in hepatocellular carcinomas. J Virol 61, 3848–3854. [Google Scholar]
  54. Tran, T. T., Trinh, T. N. & Abe, K.(2008). New complex recombinant genotype of hepatitis B virus identified in Vietnam. J Virol 82, 5657–5663.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.018127-0
Loading
/content/journal/jgv/10.1099/vir.0.018127-0
Loading

Data & Media loading...

Supplements

vol. , part 6, pp. 1609 –1620

of GenBank accession numbers of reference sequences used [ PDF] (30 KB)



PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error