Molecular epidemiology of human P[8],G9 rotaviruses in Hungary between 1998 and 2001 Free

Abstract

Increasing numbers of studies have documented the widespread distribution of human G9 rotaviruses and demonstrated that these strains may represent a fifth epidemiologically important G serotype. Serotype G9 strains were identified in Hungary for the first time in the 1997–1998 rotavirus season. Contrary to numerous surveys that reported several unexpected P–G combinations among recent G9 isolates (e.g. genotypes P[4], P[6] and P[19]), all Hungarian strains characterized to date possess the globally most common P-type, P[8], which was found among the first G9 isolates that were identified during the 1980s in the USA (WI61) and Japan (F45). To study the genetic variability within Hungarian G9 strains, RNA profile analysis and nucleotide sequencing were performed on a subset of samples that were collected between 1998 and 2001. These strains could be classified into four major RNA profiles, of which two were characteristic for epidemiologically major and two for epidemiologically minor G9 strains. Phylogenetic analysis demonstrated substantial sequence differences between the VP7 gene of Hungarian G9 strains and early strains that were isolated in the USA (WI61), Japan (F45) and India (116E) and a few recently identified isolates, e.g. from China (97'SZ37) and the USA (OM67) (<90 % nucleotide sequence similarity). In contrast, the VP7 genes of Hungarian G9 strains were related very closely to the vast majority of G9 strains that were isolated in a variety of countries over the last several years (>96 % nucleotide sequence similarity). With respect to the VP4 gene, Hungarian G9 rotaviruses fell into two of the major genetic lineages of genotype P[8], one corresponding to the epidemic strains (lineage II; P-like) and the other for two unique strains (lineage I; Wa-like), suggesting independent introduction of distinct P[8],G9 strains into Hungary or genetic reassortment between locally circulating P[8] strains and descendants of G9 isolates that were imported into the country at an earlier time. The unexpected heterogeneity found for G9 VP7 genes from several countries suggests that genetic variation among these strains has not yet been fully explored.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.45603-0
2004-08-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jmm/53/8/JM530813.html?itemId=/content/journal/jmm/10.1099/jmm.0.45603-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
    [Google Scholar]
  2. Araújo I. T., Ferreira M. S. R., Fialho A. M., Assis R. M., Cruz C. M., Rocha M., Leite J. P. G. 2001; Rotavirus genotypes P[4]G9, P[6]G9, and P[8]G9 in hospitalized children with acute gastroenteritis in Rio de Janeiro. Brazil. J Clin Microbiol 39:1999–2001 [CrossRef]
    [Google Scholar]
  3. Bányai K., Gentsch J. R., Glass R. I., Új M., Mihály I., Szücs G. 2004; Eight-year survey of human rotavirus strains demonstrates circulation of unusual G and P types in Hungary. J Clin Microbiol 42:393–397 [CrossRef]
    [Google Scholar]
  4. Bernstein D. I., Smith V. E., Sherwood J. R., Schiff G. M., Sander D. S., DeFeudis D., Spriggs D. R., Ward R. L. 1998; Safety and immunogenicity of live, attenuated human rotavirus vaccine 89-12. Vaccine 16:381–387 [CrossRef]
    [Google Scholar]
  5. Bok K., Palacios G., Sijvarger K., Matson D., Gomez J. 2001a; Emergence of G9 P[6] human rotaviruses in Argentina: phylogenetic relationships among G9 strains. J Clin Microbiol 39:4020–4025 [CrossRef]
    [Google Scholar]
  6. Bok K., Castagnaro N., Borsa A. & 8 other authors (2001b). Surveillance for rotavirus in Argentina. J Med Virol 65:190–198 [CrossRef]
    [Google Scholar]
  7. Bresee J. S., Glass R. I., Ivanoff B., Gentsch J. R. 1999; Current status and future priorities for rotavirus vaccine development, evaluation and implementation in developing countries. Vaccine 17:2207–2222 [CrossRef]
    [Google Scholar]
  8. CDC 1999a; Intussusception among recipients of rotavirus vaccine – United States, 1998–1999. Morb Mortal Wkly Rep 48:577–581
    [Google Scholar]
  9. CDC 1999b; Withdrawal of rotavirus vaccine recommendation. Morb Mortal Wkly Rep 48:1007
    [Google Scholar]
  10. Clark H. F., Hoshino Y., Bell L. M., Groff J., Hess G., Bachman P., Offit P. A. 1987; Rotavirus isolate WI61 representing a presumptive new human serotype. J Clin Microbiol 25:1757–1762
    [Google Scholar]
  11. Clark H. F., Offit P. A., Ellis R. W. & 8 other authors; 1996; The development of multivalent bovine rotavirus (strain WC3) reassortant vaccine for infants. J Infect Dis 174 (Suppl. 1):S73–S80 [CrossRef]
    [Google Scholar]
  12. Clements-Mann M. L., Dudas R., Hoshino Y. & 7 other authors; 2001; Safety and immunogenicity of live attenuated quadrivalent human–bovine (UK) reassortant rotavirus vaccine administered with childhood vaccines to infants. Vaccine 19:4676–4684 [CrossRef]
    [Google Scholar]
  13. Coulson B., Unicomb L. E., Pitson G. A., Bishop R. F. 1987; Simple and specific enzyme immunoassay using monoclonal antibodies for serotyping human rotaviruses. J Clin Microbiol 25:509–515
    [Google Scholar]
  14. Cunliffe N. A., Dove W., Bunn J. E. G., Ramadam M. B., Nyangao J. W. O., Riveron R. L., Cuevas L. E., Hart C. A. 2001a; Expanding global distribution of rotavirus serotype G9: detection in Libya, Kenya, and Cuba. Emerg Infect Dis 7:890–892 [CrossRef]
    [Google Scholar]
  15. Cunliffe N. A., Gondwe J. S., Graham S. M., Thindwa B. D. M., Dove W., Broadhead R. L., Molyneux M. E., Hart C. A. 2001b; Rotavirus strain diversity in Blantyre. Malawi: from 1997 to 1999 J Clin Microbiol 39:836–843 [CrossRef]
    [Google Scholar]
  16. Das B. K., Gentsch J. R., Hoshino Y., Ishida S., Nakagomi O., Bhan M. K., Kumar R., Glass R. I. 1993; Characterization of the G serotype and genogroup of New Delhi newborn rotavirus strain 116E. Virology 197:99–107 [CrossRef]
    [Google Scholar]
  17. Das B. K., Gentsch J. R., Cicirello H. G., Woods P. A., Gupta A., Ramachandran M., Kumar R., Bhan M. K., Glass R. I. 1994; Characterization of rotavirus strains from newborns in New Delhi, India. J Clin Microbiol 32:1820–1822
    [Google Scholar]
  18. Dolan K. T., Twist E. M., Horton-Slight P., Forrer C., Bell L. M. Jr, Plotkin S. A., Clark H. F. 1985; Epidemiology of rotavirus electropherotypes determined by a simplified diagnostic technique with RNA analysis. J Clin Microbiol 21:753–758
    [Google Scholar]
  19. Estes M. K., Cohen J. 1989; Rotavirus gene structure and function. Microbiol Rev 53:410–449
    [Google Scholar]
  20. Felsenstein J. 1989; phylip – Phylogeny inference package (version 3.2). Cladistics 5:164–166
    [Google Scholar]
  21. Flores J., Green K. Y., Garcia D. & 7 other authors; 1989; Dot hybridization assay for distinction of rotavirus serotypes. J Clin Microbiol 27:29–34
    [Google Scholar]
  22. Gentsch J. R., Glass R. I., Woods P., Gouvea V., Gorziglia M., Flores J., Das B. K., Bhan M. K. 1992; Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 30:1365–1373
    [Google Scholar]
  23. Gentsch J. R., Das B. K., Jlang B., Bhan M. K., Glass R. I. 1993; Similarity of the VP4 protein of human rotavirus strain 116E to that of the bovine B223 strain. Virology 194:424–430 [CrossRef]
    [Google Scholar]
  24. Gentsch J. R., Woods P. A., Ramachandran M., Das B. K., Leite J. P., Alfieri A., Kumar R., Bhan M. K., Glass R. I. 1996; Review of G and P typing results from a global collection of rotavirus strains: implications for vaccine development. J Infect Dis 174 (Suppl. 1):S30–S36 [CrossRef]
    [Google Scholar]
  25. Glass R. I., Bresee J. S., Parashar U. D., Holman R. C., Gentsch J. R. 1999; First rotavirus vaccine licensed: is there really a need?. Acta Paediatr Suppl 88:2–8 [CrossRef]
    [Google Scholar]
  26. Gouvea V., Santos N. 1999; Rotavirus serotype G5: an emerging cause of epidemic childhood diarrhea. Vaccine 17:1291–1292 [CrossRef]
    [Google Scholar]
  27. Gouvea V., Glass R. I., Woods P., Taniguchi K., Clark H. F., Forrester B., Fang Z.-Y. 1990; Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 28:276–282
    [Google Scholar]
  28. Gouvea V., Lima R. C. C., Linhares R. E., Clark H. F., Nosawa C. M., Santos N. 1999; Identification of two lineages (WA-like and F45-like) within the major rotavirus genotype P[8]. Virus Res 59:141–147 [CrossRef]
    [Google Scholar]
  29. Green K. Y., Hoshino Y., Ikegami N. 1989; Sequence analysis of the gene encoding the serotype-specific glycoprotein (VP7) of two new human rotavirus serotypes. Virology 168:429–433 [CrossRef]
    [Google Scholar]
  30. Griffin D. D., Kirkwood C. D., Parashar U. D., Woods P. A., Bresee J. S., Glass R. I., Gentsch J. R. & the National Rotavirus Strain Surveillance System Collaborating Laboratories; 2000; Surveillance of rotavirus strains in the United States: identification of unusual strains. J Clin Microbiol 38:2784–2787
    [Google Scholar]
  31. Hoshino Y., Kapikian A. Z. 2000; Rotavirus serotypes: classification and importance in epidemiology, immunity, and vaccine development. J Health Popul Nutr 18:5–14
    [Google Scholar]
  32. Iturriza-Gómara M., Green J., Brown D. W. G., Ramsay M., Desselberger U., Gray J. J. 2000; Molecular epidemiology of human group A rotavirus infections in the United Kingdom between 1995 and 1998. J Clin Microbiol 38:4394–4401
    [Google Scholar]
  33. Iturriza-Gómara M., Isherwood B., Desselberger U., Gray J. 2001; Reassortment in vivo: driving force for diversity of human rotavirus strains isolated in the United Kingdom between 1995 and 1999. J Virol 75:3696–3705 [CrossRef]
    [Google Scholar]
  34. Iturriza-Gòmara M., Anderton E., Kang G., Gallimore C., Phillips W., Desselberger U., Gray J. 2003; Evidence for genetic linkage between the gene segments encoding NSP4 and VP6 proteins in common and reassortant human rotavirus strains. J Clin Microbiol 41:3566–3573 [CrossRef]
    [Google Scholar]
  35. Jagannath M. R., Vethanayagam R. R., Reddy B. S. Y., Raman S., Rao C. D. 2000; Characterization of human symptomatic rotavirus isolates MP409 and MP480 having ‘long’ RNA electropherotype and subgroup I specificity, highly related to the P6[1],G8 type bovine rotavirus A5, from Mysore, India. Arch Virol 145:1339–1357 [CrossRef]
    [Google Scholar]
  36. Jain V., Das B. K., Bhan M. K., Glass R. I., Gentsch J. R. & the Indian Strain Surveillance Collaborating Laboratories; 2001; Great diversity of group A rotavirus strains and high prevalence of mixed rotavirus infections in India. J Clin Microbiol 39:3524–3529 [CrossRef]
    [Google Scholar]
  37. Kapikian A. Z., Chanock R. M. 1996; Rotaviruses. In Fields Virology , 3rd edn. vol2 pp 1657–1708 Edited by Fields B. N., Knipe D. N., Howley P. M., Chanock R. M., Melnick J. L., Monath T. P., Roizman B., Straus S. E. New York: Lippincott-Raven;
    [Google Scholar]
  38. Kumar S., Tamura K., Jakobsen I. B., Nei M. 2001; mega2: molecular evolutionary genetic analysis software. Bioinformatics 17:1244–1245 [CrossRef]
    [Google Scholar]
  39. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
    [Google Scholar]
  40. Laird A. R., Gentsch J. R., Nakagomi T., Nakagomi O., Glass R. I. 2003; Characterization of serotype G9 rotavirus strains isolated in the United States and India from 1993 to 2001. J Clin Microbiol 41:3100–3111 [CrossRef]
    [Google Scholar]
  41. Larralde G., Flores J. 1990; Identification of gene 4 alleles among human rotaviruses by polymerase chain reaction-derived probes. Virology 179:469–473 [CrossRef]
    [Google Scholar]
  42. Li G., Jing Y., Qian Y. 1997; Sequence analysis of the gene encoding VP7 from a rotavirus serotype 9 field strain. Bingdu Xuebao 13:376–381
    [Google Scholar]
  43. Martella V., Terio V., Del Gaudio G., Gentile M., Fiorente P., Barbuti S., Buonavoglia C. 2003; Detection of the emerging rotavirus G9 serotype at high frequency in Italy. J Clin Microbiol 41:3960–3963 [CrossRef]
    [Google Scholar]
  44. Maunula L., von Bonsdorff C.-H. 1998; Short sequences define genetic lineages: phylogenetic analysis of group A rotaviruses based on partial sequences of genome segments 4 and 9. J Gen Virol 79:321–332
    [Google Scholar]
  45. Maunula L., von Bonsdorff C.-H. 2002; Frequent reassortments may explain the genetic heterogeneity of rotaviruses: analysis of Finnish rotavirus strains. J Virol 76:11793–11800 [CrossRef]
    [Google Scholar]
  46. Midthun K., Greenberg H. B., Hoshino Y., Kapikian A. Z., Wyatt R. G., Chanock R. M. 1985; Reassortant rotaviruses as potential live rotavirus vaccine candidates. J Virol 53:949–954
    [Google Scholar]
  47. Muñoz M., Lanza I., Álvarez M., Cármenes P. 1995; Prevalence of neutralizing antibodies to 9 rotavirus strains representing 7 G-serotypes in sheep sera. Vet Microbiol 45:351–361 [CrossRef]
    [Google Scholar]
  48. Nakagomi T., Akatani K., Ikegami N., Katsushima N., Nakagomi O. 1988; Occurrence of changes in human rotavirus serotypes with concurrent changes in genomic RNA electropherotypes. J Clin Microbiol 26:2586–2592
    [Google Scholar]
  49. Nakagomi T., Ohshima A., Akatani K., Ikegami N., Katsushima N., Nakagomi O. 1990; Isolation and molecular characterization of a serotype 9 human rotavirus strain. Microbiol Immunol 34:77–82 [CrossRef]
    [Google Scholar]
  50. Nakagomi O., Isegawa Y., Ward R. L., Knowlton D. R., Kaga E., Nakagomi T., Ueda S. 1994; Naturally occurring dual infection with human and bovine rotaviruses as suggested by the recovery of G1P8 and G1P5 rotaviruses from a single patient. Arch Virol 137:381–388 [CrossRef]
    [Google Scholar]
  51. Nguyen V. M., Nguyen V. T., Huynh P. L. 8 other authors; 2001; The epidemiology and disease burden of rotavirus in Vietnam: sentinel surveillance at 6 hospitals. J Infect Dis 183:1707–1712 [CrossRef]
    [Google Scholar]
  52. Nicholas K. B., Nicholas H. B. Jr, Deerfield D. W. II 1997; GeneDoc: analysis and visualization of genetic variation. Embnet News 4:1–4
    [Google Scholar]
  53. O'Halloran F., Lynch M., Cryan B., Fanning S. 2002; Application of restriction fragment length polymorphism analysis of VP7-encoding genes: fine comparison of Irish and global rotavirus isolates. J Clin Microbiol 40:524–531 [CrossRef]
    [Google Scholar]
  54. Oka T., Nakagomi T., Nakagomi O. 2000; Apparent re-emergence of serotype G9 in 1995 among rotaviruses recovered from Japanese children hospitalized with acute gastroenteritis. Microbiol Immunol 44:957–961 [CrossRef]
    [Google Scholar]
  55. Okada J., Urasawa T., Kobayashi N., Taniguchi K., Hasegawa A., Mise K., Urasawa S. 2000; New P serotype of group A human rotavirus closely related to that of a porcine rotavirus. J Med Virol 60:63–69 [CrossRef]
    [Google Scholar]
  56. Palombo E. A., Masendycz P. J., Bugg H. C., Bogdanovic-Sakran N., Barnes G. L., Bishop R. F. 2000; Emergence of serotype G9 human rotaviruses in Australia. J Clin Microbiol 38:1305–1306
    [Google Scholar]
  57. Ramachandran M., Das B. K., Vij A. & 10 other authors; 1996; Unusual diversity of human rotavirus G and P genotypes in India. J Clin Microbiol 34:436–439
    [Google Scholar]
  58. Ramachandran M., Kirkwood C. D., Unicomb L., Cunliffe N. A., Ward R. L., Bhan M. K., Clark H. F., Glass R. I., Gentsch J. R. 2000; Molecular characterization of serotype G9 rotavirus strains from a global collection. Virology 278:436–444 [CrossRef]
    [Google Scholar]
  59. Santos N., Lima R. C. C., Nozawa C. M., Linhares R. E., Gouvea V. 1999; Detection of porcine rotavirus type G9 and of a mixture of types G1 and G5 associated with Wa-like VP4 specificity: evidence for natural human-porcine genetic reassortment. J Clin Microbiol 37:2734–2736
    [Google Scholar]
  60. Taniguchi K., Urasawa T., Morita Y., Greenberg H. B., Urasawa S. 1987; Direct serotyping of human rotavirus in stools by an enzyme-linked immunosorbent assay using serotype 1-, 2-, 3-, and 4-specific monoclonal antibodies to VP7. J Infect Dis 155:1159–1166 [CrossRef]
    [Google Scholar]
  61. Unicomb L. E., Podder G., Gentsch J. R., Woods P. A., Hasan K. Z., Faruque A. S. G., Albert M. J., Glass R. I. 1999; Evidence of high-frequency genomic reassortment of group A rotavirus strains in Bangladesh: emergence of type G9 in 1995. J Clin Microbiol 37:1885–1891
    [Google Scholar]
  62. Urasawa S., Hasegawa A., Urasawa T. & 10 other authors; 1992; Antigenic and genetic analyses of human rotaviruses in Chiang Mai, Thailand: evidence for a close relationship between human and animal rotaviruses. J Infect Dis 166:227–234 [CrossRef]
    [Google Scholar]
  63. Widdowson M.-A., van Doornum G. J. J., van der Poel W. H. M., de Boer A. S., Mahdi U., Koopmans M. 2000; Emerging group-A rotavirus and a nosocomial outbreak of diarrhoea. Lancet 356:1161–1162 [CrossRef]
    [Google Scholar]
  64. Wyatt R. G., James H. D. Jr, Pittman A. L., Hoshino Y., Greenberg H. B., Kalica A. R., Flores J., Kapikian A. Z. 1983; Direct isolation in cell culture of human rotaviruses and their characterization into four serotypes. J Clin Microbiol 18:310–317
    [Google Scholar]
  65. Xia X., Xie Z. 2001; dambe: software package for data analysis in molecular biology and evolution. J Hered 92:371–373 [CrossRef]
    [Google Scholar]
  66. Zhou Y., Supawadee J., Khamwan C. & 9 other authors; 2001; Characterization of human rotavirus serotype G9 isolated in Japan and Thailand from 1995 to 1997. J Med Virol 65:619–628 [CrossRef]
    [Google Scholar]
  67. Zhou Y., Li L., Okitsu S., Maneekarn N., Ushijima H. 2003; Distribution of human rotaviruses, especially G9 strains, in Japan from 1996 to 2000. Microbiol Immunol 47:591–599 [CrossRef]
    [Google Scholar]
  68. Zizdic S., Ridjanovic Z., Masic I. 1992; Newly discovered rotavirus serotypes in 4 years of collecting samples from children with diarrheal syndromes. Medicinski Arhiv 45:15–18
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.45603-0
Loading
/content/journal/jmm/10.1099/jmm.0.45603-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed