1887

Abstract

Variants of hepatitis C virus (HCV) have been classified by nucleotide sequence comparisons in different regions of the genome. Many investigators have defined the ranges of sequence similarity values or evolutionary distances corresponding to divisions of HCV into types, subtypes and isolates. Using these criteria, novel variants of HCV from Vietnam, Thailand and Indonesia have been classified as types 7, 8, 9, 10 and 11, many of which can be further subdivided into between two to four subtypes. In this study, this distance-based method of virus classification was compared with phylogenetic analysis and statistical measures to establish the confidence of the groupings. Using bootstrap resampling of phylogenetic trees in several subgenomic regions (core, E1, NS5) and with complete genomic sequences, we found that one set of novel HCV variants (‘types 7, 8, 9 and 11’) consistently grouped together into a single clade that also contained type 6a, while ‘type 10a’ grouped with type 3. In contrast, no robust higher-order groupings were observed between any of the other five previously described HCV genotypes (types 1–5). In each subgenomic region, the distribution of pairwise distances between members of the type 6 clade were consistently bi-modal and therefore provided no justification for classification of these variants into the three proposed categories (type, subtype, isolate). Based on these results, we propose that a more useful classification would regard all these variants as subtypes of type 6 or type 3, even though the level of sequence diversity within the clade was greater than observed for other genotypes. Classification by phylogenetic relatedness rules out simple sequence similarity measurements as a method for assigning HCV genotypes, but provides a more appropriate description of the evolutionary and epidemiological history of a virus.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-77-12-3013
1996-12-01
2021-10-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/77/12/JV0770123013.html?itemId=/content/journal/jgv/10.1099/0022-1317-77-12-3013&mimeType=html&fmt=ahah

References

  1. Apichartpiyakul C., Chittivudikarn C., Miyajima H., Homma M., Hotta H. 1994; Analysis of hepatitis C virus isolates among healthy blood donors and drug addicts in Chiang Mai, Thailand. Journal of Clinical Microbiology 32:2276–2279
    [Google Scholar]
  2. Bhattacherjee V., Prescott L. E., Pike I., Rodgers B., Bell H., Elzayadi A. R., Kew M. C., Conradie J., Lin C. K., Marsden H., Saeed A. A., Parker D., Yap P. L., Simmonds P. 1995; Use of NS-4 peptides to identify type-specific antibody to hepatitis C virus genotypes 1, 2, 3, 4, 5 and 6. Journal of General Virology 76:1737–1748
    [Google Scholar]
  3. Bukh J. 1995; Genetic heterogeneity of hepatitis C virus: quasispecies and genotypes. Seminars in Liver Disease 15:41–63
    [Google Scholar]
  4. Bukh J., Miller R. H. 1994; Diagnostic and clinical implications of the different genotypes of hepatitis C virus. Hepatology 20:256–259
    [Google Scholar]
  5. Bukh J., Purcell R. H., Miller R. H. 1993; At least 12 genotypes of hepatitis C virus predicted by sequence analysis of the putative E1 gene of isolates collected worldwide. Proceedings of the National Academy of Sciences, USA 90:8234–8238
    [Google Scholar]
  6. Bukh J., Purcell R. H., Miller R. H. 1994; Sequence analysis of the core gene of 14 hepatitis C virus genotypes. Proceedings of the National Academy of Sciences, USA 91:8239–8243
    [Google Scholar]
  7. Choo Q. L., Richman K. H., Han J. H., Berger K., Lee C., Dong C., Gallegos C., Coit D., Medina Selby R., Barr P. J., Weiner A. J., Bradley D. W., Kuo G., Houghton M. 1991; Genetic organization and diversity of the hepatitis C virus. Proceedings of the National Academy of Sciences, USA 88:2451–2455
    [Google Scholar]
  8. Davis G. L. 1994; Prediction of response to interferon treatment of chronic hepatitis C. Journal of Hepatology 21:1–3
    [Google Scholar]
  9. Doi H., Apichartpiyakul C., Ohba K. I., Mizokami M., Hotta H. 1996; Hepatitis C virus (HCV) subtype prevalence in Chaing Mai, Thailand and identification of novel subtypes of HCV in major type 6. Journal of Clinical Microbiology 34:569–574
    [Google Scholar]
  10. Felsenstein J. 1993 PHYLIP inference package version 3.5. Seattle: Department of Genetics, University of Washington;
    [Google Scholar]
  11. Felsenstein J., Kishino H. 1993; Is there something wrong with bootstrap on phytogenies? A reply to Hillis and Bull. Systematic Biology 42:193–200
    [Google Scholar]
  12. Hillis D. M., Bull J. J. 1993; An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42:182–192
    [Google Scholar]
  13. Holmes E. C., Nee S., Rambaut A., Garnett G. P., Harvey P. H. 1995; Revealing the history of infectious disease epidemics using phylogenetic trees. Philosophical Transactions of the Royal Society of London Series B Biological Sciences 349:33–40
    [Google Scholar]
  14. Hotta H., Doi H., Hayashi T., Purwanta M., Soemarto W., Mizokami M., Ohba K., Homma M. 1994a; Analysis of the core and e1 envelope region sequences of a novel variant of hepatitis C virus obtained in Indonesia. Archives of Virology 136:53–62
    [Google Scholar]
  15. Hotta H., Handajani R., Lusida M. I., Soemarto W., Doi H., Miyajima H., Homma M. 1994b; Subtype analysis of hepatitis C virus in Indonesia on the basis of NS5b region sequences. Journal of Clinical Microbiology 32:3049–3051
    [Google Scholar]
  16. Lau J. Y. N., Davis G. L., Prescott L. E., Maertens G., Lindsay K. L., Qian K. P., Mizokami M., Simmonds P., Perrillo R. P., Schiff E. R., Bodenheimer H. C., Balart L. A., Regenstein F., Dienstag J. L., Katkov W. N., Tamburro C. H., Goff J. S., Everson G. T., Goodman Z., Albrecht J. 1996; Distribution of hepatitis C virus genotypes determined by line probe assay in patients with chronic hepatitis C seen at tertiary referral centers in the United States. Annals of Internal Medicine 124:868
    [Google Scholar]
  17. Li W. H., Zharkikh A. 1994; What is the bootstrap technique?. Systematic Biology 43:424–430
    [Google Scholar]
  18. Mahaney K., Tedeschi V., Maertens G., Dibisceglie A. M., Vergalla J., Hoofnagle J. H., Sallie R. 1994; Genotypic analysis of hepatitis C virus in American patients. Hepatology 20:1405–1411
    [Google Scholar]
  19. McOmish F., Chan S.-W., Dow B. C., Gillon J., Frame W. D., Crawford R. J., Yap P. L., Fotlett E. A. C., Simmonds P. 1993; Detection of three types of hepatitis C virus in blood donors: investigation of type-specific differences in serological reactivity and rate of alanine aminotransferase abnormalities. Transfusion 33:7–13
    [Google Scholar]
  20. Mellor J., Holmes E. C., Jarvis L. M., Yap P.-L., Simmonds P. The International HCV Collaborative Study Group 1995; Investigation of the pattern of hepatitis C virus sequence diversity in different geographical regions: implications for virus classification. Journal of General Virology 76:2493–2507
    [Google Scholar]
  21. Mellor J., Walsh E. A., Prescott L. E., Jarvis L. M., Davidson F., Yap P. L., Simmonds P., Nowicki M. J., Mosley J. W., Lin C. K., Lai C. L., Deolim G., Martins I. A., Ong Y. W., Teo D., Lin M., Nuchprayoon C., Tanprasert S. 1996; Survey of type 6 group variants of hepatitis C virus in southeast Asia by using a core-based genotyping assay. Journal of Clinical Microbiology 34:417–423
    [Google Scholar]
  22. Miyakawa Y., Okamoto H., Mayumi M. 1995; Classifying hepatitis C virus genotypes. Molecular Medicine Today 1:20–25
    [Google Scholar]
  23. Sakamoto M., Akahane Y., Tsuda F., Tanaka T., Woodfield D. G., Okamoto H. 1994; Entire nucleotide sequence and characterization of a hepatitis C virus of genotype v/3a. Journal of General Virology 75:1761–1768
    [Google Scholar]
  24. Simmonds P., Holmes E. C., Cha T. A., Chan S.-W., McOmish F., Irvine B., Beall E., Yap P. L., Kolberg J., Urdea M. S. 1993; Classification of hepatitis C virus into six major genotypes and a series of subtypes by phylogenetic analysis of the NS-5 region. Journal of General Virology 74:2391–2399
    [Google Scholar]
  25. Simmonds P., Alberti A., Alter H. J., Bonino F., Bradley D. W., Brechot C., Brouwer J. T., Chan S. W., Chayama K., Chen D. S., Choo Q. L., Colombo M., Cuypers H. T. M., Date T., Dusheiko G. M., Esteban J. I., Fay O., Hadziyannis S. J., Han J., Hatzakis E. C., Hotta H., Houghton M., Irvine B., Kohara M., Kolberg J. A., Kuo G., Lau J. Y. N., Date T., Lelie P. N., Maertens G., McOmish F., Miyamura T., Mizokami M., Nomoto A., Prince, A. M., Reesink H. W., Rice C., Roggendorf M., Schalm S. W., Shikata T. 1994a; A proposed system for the nomenclature of hepatitis C viral genotypes. Hepatology 19:1321–1324
    [Google Scholar]
  26. Simmonds P., Smith D.B, Comish F., Yap P. L., Kolberg J., Urdea M.S., Schalm S. W., Shikata T., Holmes E. C. 1994b; Identification of genotypes of hepatitis C virus by sequence comparisons in the core, E1 and NS-5 regions. Journal of General Virology 75:1053–1061
    [Google Scholar]
  27. Smith D. B., Mellor J., Jarvis L. M., Davidson F., Kolberg J., Urdea M., Yap P.-L., Simmonds P. The International HCV Collaborative Study Group 1995; Variation of the hepatitis C virus 5’ non-coding region: implications for secondary structure, virus detection and typing. Journal of General Virology 76:1749–1761
    [Google Scholar]
  28. Stuyver L., Vanarnhem W., Wyseur A., Hernandez F., Delaporte E., Maertens G. 1994; Classification of hepatitis C viruses based on phylogenetic analysis of the envelope 1 and nonstructural 5b regions and identification of five additional subtypes. Proceedings of the National Academy of Sciences, USA 91:10134–10138
    [Google Scholar]
  29. Sugiyama K., Kato N., Nakazawa T., Yonemura Y., Phornphutkul K., Kunakorn M., Petehdai B., Shimotohno K. 1995; Novel genotypes of hepatitis C virus in Thailand. Journal of General Virology 76:2323–2327
    [Google Scholar]
  30. Tokita H., Okamoto H., Tsuda F., Song P., Nakata S., Chosa T., Lizuka H., Mishiro S., Miyakawa Y., Mayumi M. 1994; Hepatitis C virus variants from Vietnam are classifiable into the seventh, eighth, and ninth major genetic groups. Proceedings of the National Academy of Sciences, USA 91:11022–11026
    [Google Scholar]
  31. Tokita H., Okamoto H., Luengrojanakul P., Vareesangthip K., Chainuvati T., Lizuka H., Tsuda F., Miyakawa Y., Mayumi M. 1995; Hepatitis C virus variants from Thailand classifiable into five novel genotypes in the sixth (6b), seventh (7c, 7d) and ninth (9b, 9c) major genetic groups. Journal of General Virology 76:2329–2335
    [Google Scholar]
  32. Tokita H., Okamoto H., Lizuka H., Kishimoto J., Tsuda F., Lesmana A., Miyakawa Y., Mayumi M. 1996; Hepatitis C virus variants from Jakarta, Indonesia classifiable into novel genotypes in the second (2e and 2f), tenth (10a) and eleventh (11a) genetic groups. Journal of General Virology 77:293–301
    [Google Scholar]
  33. Tsukiyama Kohara K., Yamaguchi K., Maki N., Ohta Y., Miki K., Mizokami M., Ohba K., Tanaka S., Hattori N., Nomoto A., Kohara M. 1993; Antigenicities of group I and group II hepatitis C virus polypeptides-molecular basis of diagnosis. Virology 192:430–437
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-77-12-3013
Loading
/content/journal/jgv/10.1099/0022-1317-77-12-3013
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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