Molecular characterization of hepatitis B virus in liver disease patients and asymptomatic carriers of the virus in Sudan

BMC Infectious Diseases

Volumn 13, Issue 1, 2013, Pages

  Yousif, Mukhlid ^a   Mudawi, Hatim ^b   Bakhiet, Sahar ^c   Glebe, Dieter ^d   Kramvis, Anna ^a  

^a UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^b UNIVERSITY OF KHARTOUM   (Sudan)

^c UNIVERSITY OF KHARTOUM   (Sudan)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Africa; Bioinformatics; Genotype; Phylogenetics; Serotype; Subgenotype; Sudan

Indexed keywords

ALANINE AMINOTRANSFERASE; HEPATITIS B(E) ANTIGEN; VIRUS DNA;

ACUTE HEPATITIS; ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANTIGEN DETECTION; ARTICLE; ASYMPTOMATIC DISEASE; CHRONIC HEPATITIS; CONTROLLED STUDY; DELETION MUTANT; FEMALE; GENE SEQUENCE; GENOTYPE; HEPATITIS B VIRUS; HUMAN; LIVER CELL CARCINOMA; MAJOR CLINICAL STUDY; MALE; NUCLEOTIDE SEQUENCE; PROMOTER REGION; SUDAN; UNINDEXED SEQUENCE; VIRUS CARRIER; VIRUS LOAD;

EID: 84880182698     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/1471-2334-13-328     Document Type: Article

References (53)

1. WHO Hepatitis B virus Fact sheet N° 204 2012, http://www.who.int/mediacentre/factsheets/fs204/en/. Accessed January 2013, WHO.
2. Kramvis A, Kew MC. Epidemiology of hepatitis B virus in Africa, its genotypes and clinical associations of genotypes. Hepatol Res 2007, 37(s1):S9-S19. 10.1111/j.1872-034X.2007.00098.x, 17627641.
3. Mudawi HMY. Epidemiology of viral hepatitis in Sudan. Clin Exp Gastroenterol 2008, 1:9-13. 3108625, 21677820.
4. Mudawi HM, Smith HM, Rahoud SA, Fletcher IA, Saeed OK, Fedail SS. Prevalence of hepatitis B virus infection in the Gezira state of central Sudan. Saudi J Gastroenterol 2007, 13(2):81-83. 10.4103/1319-3767.32182, 19858618.
5. McCarthy MC, El-Tigani A, Khalid IO, Hyams KC. Hepatitis B and C in Juba, southern Sudan: results of a serosurvey. Trans R Soc Trop Med Hyg 1994, 88(5):534-536. 10.1016/0035-9203(94)90150-3, 7992329.
6. McCarthy MC, Hyams KC, el-Tigani el-Hag A, el-Dabi MA, el-Sadig el-Tayeb M, Khalid IO, George JF, Constantine NT, Woody JN. HIV-1 and hepatitis B transmission in Sudan. AIDS 1989, 3(11):725-729. 10.1097/00002030-198911000-00006, 2515878.
7. Mudawi HMY, Yousif BA. Fulminant hepatic failure in an African setting: Etiology, clinical course, and predictors of mortality. Dig Dis Sci 2007, 52:3266-3269. 10.1007/s10620-006-9730-z, 17436091.
8. Mahgoub S, Candotti D, El-Ekiaby M, Allain JP. Hepatitis B virus (HBV) infection and recombination between HBV genotypes D and E in asymptomatic blood donors from Khartoum Sudan. J Clin Microbiol 2011, 49(1):298-306. 10.1128/JCM.00867-10, 3020474, 21048009.
9. Kramvis A, Kew M, Francois G. Hepatitis B virus genotypes. Vaccine 2005, 23(19):2409-2423. 10.1016/j.vaccine.2004.10.045, 15752827.
10. Norder H, Courouce AM, Coursaget P, Echevarria JM, Lee SD, Mushahwar IK, Robertson BH, Locarnini S, Magnius LO. Genetic diversity of hepatitis B virus strains derived worldwide: genotypes, subgenotypes, and HBsAg subtypes. Intervirology 2004, 47(6):289-309. 10.1159/000080872, 15564741.
11. Yu H, Yuan Q, Ge SX, Wang HY, Zhang YL, Chen QR, Zhang J, Chen PJ, Xia NS. Molecular and phylogenetic analyses suggest an additional hepatitis B virus genotype " I". PLoS One 2010, 5(2):e9297. 10.1371/journal.pone.0009297, 2824819, 20174575.
12. Tatematsu K, Tanaka Y, Kurbanov F, Sugauchi F, Mano S, Maeshiro T, Nakayoshi T, Wakuta M, Miyakawa Y, Mizokami M. 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 2009, 83(20):10538-10547. 10.1128/JVI.00462-09, 2753143, 19640977.
13. Saudy N, Sugauchi F, Tanaka Y, Suzuki S, Aal AA, Zaid MA, Agha S, Mizokami M. Genotypes and phylogenetic characterization of hepatitis B and delta viruses in Egypt. J Med Virol 2003, 70(4):529-536. 10.1002/jmv.10427, 12794714.
14. Mulders MN, Venard V, Njayou M, Edorh AP, Bola Oyefolu AO, Kehinde MO, Muyembe Tamfum JJ, Nebie YK, Maiga I, Ammerlaan W, et al. Low genetic diversity despite hyperendemicity of hepatitis B virus genotype E throughout West Africa. J Infect Dis 2004, 190(2):400-408. 10.1086/421502, 15216479.
15. Mwangi J, Nganga Z, Songok E, Kinyua J, Lagat N, Muriuki J, Lihana R, Khamadi S, Osman S, Lwembe R, et al. Molecular genetic diversity of hepatitis B virus in Kenya. Intervirology 2008, 51(6):417-421. 10.1159/000205526, 19258721.
16. Usuda S, Okamoto H, Tanaka T, Kidd-Ljunggren K, Holland PV, Miyakawa Y, Mayumi M. Differentiation of hepatitis B virus genotypes D and E by ELISA using monoclonal antibodies to epitopes on the preS2-region product. J Virol Methods 2000, 87(1-2):81-89.
17. Hannoun C, Soderstrom A, Norkrans G, Lindh M. 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 2005, 86(Pt 8):2163-2167.
18. Kramvis A, Kew MC. Relationship of genotypes of hepatitis B virus to mutations, disease progression and response to antiviral therapy. J Viral Hepat 2005, 12(5):456-464. 10.1111/j.1365-2893.2005.00624.x, 16108759.
19. Kao JH, Chen PJ, Lai MY, Chen DS. Genotypes and clinical phenotypes of hepatitis B virus in patients with chronic hepatitis B virus infection. J Clin Microbiol 2002, 40(4):1207-1209. 10.1128/JCM.40.4.1207-1209.2002, 140384, 11923332.
20. Mohsni E. HBV and HCV Contorl in the WHO Eastern Mediterranean Region (WHO EMR). Viral Hepatitis 2010, 18(2):26-27.
21. Papatheodoridis GV, Manolakopoulos S, Liaw YF, Lok A. Follow-up and indications for liver biopsy in HBeAg-negative chronic hepatitis B virus infection with persistently normal ALT: a systematic review. J Hepatol 2012, 57(1):196-202. 10.1016/j.jhep.2011.11.030, 22450396.
22. Weinberger KM, Wiedenmann E, Bohm S, Jilg W. Sensitive and accurate quantitation of hepatitis B virus DNA using a kinetic fluorescence detection system (TaqMan PCR). J Virol Methods 2000, 85(1-2):75-82.
23. Firnhaber C, Viana R, Reyneke A, Schultze D, Malope B, Maskew M, Di-Bisceglie A, MacPhail P, Sanne I, Kew M. Occult hepatitis B virus infection in patients with isolated core antibody and HIV co-infection in an urban clinic in Johannesburg South Africa. Int J Infect Dis 2009, 13(4):488-492. 10.1016/j.ijid.2008.08.018, 3016468, 19081280.
24. Firnhaber C, Chen CY, Evans D, Maskew M, Schulz D, Reyneke A, Kramvis A. Prevalence of hepatitis B virus (HBV) co-infection in HBV serologically-negative South African HIV patients and retrospective evaluation of the clinical course of mono- and co-infection. Int J Infect Dis 2012, 16(4):e268-e272. 10.1016/j.ijid.2011.12.007, 22305987.
25. Bell TG, Makondo E, Martinson NA, Kramvis A. Hepatitis B virus infection in human immunodeficiency virus infected southern African adults: occult or overt-that is the question. PLoS One 2012, 7(10):e45750. 10.1371/journal.pone.0045750, 3462206, 23049685.
26. Takahashi K, Aoyama K, Ohno N, Iwata K, Akahane Y, Baba K, Yoshizawa H, Mishiro S. The precore/core promoter mutant (T1762A1764) of hepatitis B virus: clinical significance and an easy method for detection. J Gen Virol 1995, 76(Pt 12):3159-3164.
27. Vermeulen M, Dickens C, Lelie N, Walker E, Coleman C, Keyter M, Reddy R, Crookes R, Kramvis A. Hepatitis B virus transmission by blood transfusion during 4 years of individual-donation nucleic acid testing in South Africa: estimated and observed window period risk. Transfusion 2012, 52:880-892. 10.1111/j.1537-2995.2011.03355.x, 21981386.
28. Kew MC, Kramvis A, Yu MC, Arakawa K, Hodkinson J. Increased hepatocarcinogenic potential of hepatitis B virus genotype A in Bantu-speaking sub-saharan Africans. J Med Virol 2005, 75(4):513-521. 10.1002/jmv.20311, 15714494.
29. Lindh M, Andersson AS, Gusdal A. Genotypes, nt 1858 variants, and geographic origin of hepatitis B virus-large-scale analysis using a new genotyping method. J Infect Dis 1997, 175(6):1285-1293. 10.1086/516458, 9180165.
30. Gunther S, Li BC, Miska S, Kruger DH, Meisel H, Will H. 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 1995, 69(9):5437-5444. 189390, 7636989.
31. Makondo E, Bell TG, Kramvis A. Genotyping and Molecular Characterization of Hepatitis B Virus from Human Immunodeficiency Virus-Infected Individuals in Southern Africa. PLoS One 2012, 7(9):e46345. 46310.41371/journal.pone.0046345, 3460816, 23029487.
32. Bell TG, Kramvis A. Fragment merger: an online tool to merge overlapping long sequence fragments. Viruses 2013, 5(3):824-833. 10.3390/v5030824, 3705298, 23482300.
33. Yousif M, Kramvis A. Genotype D of hepatitis B virus and its subgenotypes: An update. Hepatol Res 2013, 43(4):355-364. 10.1111/j.1872-034X.2012.01090.x, 22978460.
34. Gulube Z, Chirara M, Kew M, Tanaka Y, Mizokami M, Kramvis A. Molecular characterization of hepatitis B virus isolates from Zimbabwean blood donors. J Med Virol 2011, 83(2):235-244. 10.1002/jmv.21954, 21181917.
35. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 1999, 73(1):152-160. 103818, 9847317.
36. Bell TG, Kramvis A. Mutation Reporter Tool: An online tool to interrogate loci of interest, with its utility demonstrated using hepatitis B virus. Virol J 2013, 10(1):62. 10.1186/1743-422X-10-62, 23433201.
37. Liaw Y-F, Chien R-N, Yeh C-T, Tsai S-L, Chu C-M. Acute exacerbation and hepatitis B virus clearance after emergence of YMDD motif mutation during lamivudine therapy. Hepatology 1999, 30(2):567-572. 10.1002/hep.510300221, 10421670.
38. Rehermann B, Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat Rev Immunol 2005, 5(3):215-229. 10.1038/nri1573, 15738952.
39. Liu TT, Fang Y, Xiong H, Chen TY, Ni ZP, Luo JF, Zhao NQ, Shen XZ. A case-control study of the relationship between hepatitis B virus DNA level and risk of hepatocellular carcinoma in Qidong China. World J Gastroenterol 2008, 14(19):3059-3063. 10.3748/wjg.14.3059, 2712175, 18494059.
40. Abdou Chekaraou M, Brichler S, Mansour W, Le-Gal F, Garba A, Deny P, Gordien E. A novel hepatitis B virus (HBV) subgenotype D (D8) strain, resulting from recombination between genotypes D and E, is circulating in Niger along with HBV/E strains. J Gen Virol 2010, 91(Pt 6):1609-1620.
41. Kramvis A, Arakawa K, Yu MC, Nogueira R, Stram DO, Kew MC. Relationship of serological subtype, basic core promoter and precore mutations to genotypes/subgenotypes of hepatitis B virus. J Med Virol 2008, 80(1):27-46. 10.1002/jmv.21049, 18041043.
42. Kramvis A, Paraskevis D. Subgenotype A1 of Hepatitis B Virus - Tracing Human Migrations in and out of Africa. Antivir Ther 2013, 18(3 Pt B):513-521. 10.3851/IMP2657, 23792935.
43. Milich D, Liang TJ. Exploring the biological basis of hepatitis B e antigen in hepatitis B virus infection. Hepatology 2003, 38(5):1075-1086. 10.1053/jhep.2003.50453, 14578844.
44. Carman WF, Jacyna MR, Hadziyannis S, Karayiannis P, McGarvey MJ, Makris A, Thomas HC. Mutation preventing formation of hepatitis B e antigen in patients with chronic hepatitis B infection. Lancet 1989, 2(8663):588-591.
45. Li JS, Tong SP, Wen YM, Vitvitski L, Zhang Q, Trepo C. Hepatitis B virus genotype A rarely circulates as an HBe-minus mutant: possible contribution of a single nucleotide in the precore region. J Virol 1993, 67(9):5402-5410. 237941, 8350403.
46. Lok AS, Akarca U, Greene S. 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 1994, 91(9):4077-4081. 10.1073/pnas.91.9.4077, 43726, 8171038.
47. Ahn SH, Kramvis A, Kawai S, Spangenberg HC, Li J, Kimbi G, Kew M, Wands J, Tong S. Sequence variation upstream of precore translation initiation codon reduces hepatitis B virus e antigen production. Gastroenterology 2003, 125(5):1370-1378. 10.1016/j.gastro.2003.07.016, 14598253.
48. Garmiri P, Loua A, Haba N, Candotti D, Allain JP. 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 2009, 90(Pt 10):2442-2451.
49. Chen BF, Liu CJ, Jow GM, Chen PJ, Kao JH, Chen DS. High Prevalence and Mapping of Pre-S Deletion in Hepatitis B Virus Carriers With Progressive Liver Diseases. Gastroenterology 2006, 130(4):1153-1168. 10.1053/j.gastro.2006.01.011, 16618410.
50. Mun H-S, Lee S-A, Kim H, Hwang E-S, Kook Y-H, Kim B-J. Novel F141L Pre-S2 Mutation in Hepatitis B Virus Increases the Risk of Hepatocellular Carcinoma in Patients with Chronic Genotype C Infections. J Virol 2011, 85(1):123-132. 10.1128/JVI.01524-10, 3014212, 20962085.
51. Biswas A, Panigrahi R, Banerjee A, Pal M, De BK, Chakrabarti S, Chakravarty R. Differential pattern of pre-S mutations/deletions and its association with hepatitis B virus genotypes in Eastern India. Infect Genet Evol 2012, 12(2):384-391. 10.1016/j.meegid.2012.01.007, 22266243.
52. Carman WF. The clinical significance of surface antigen variants of hepatitis B virus. J Viral Hepat 1997, 4(Suppl 1):11-20.
53. Dupouey J, Gerolami R, Solas C, Colson P. Hepatitis B virus variant with the a194t substitution within reverse transcriptase before and under adefovir and tenofovir therapy. Clinics and Research in Hepatology and Gastroenterology 2012, 36(2):e26-e28. 10.1016/j.clinre.2012.01.003, 22342116.