1887

Journal of General Virology header logo

Volume 94, Issue 6

G8 rotaviruses with conserved genotype constellations detected in Malawi over 10 years (1997–2007) display frequent gene reassortment among strains co-circulating in humans Open Access

Abstract

Rotavirus A, the most common cause of severe diarrhoea in children worldwide, occurs in five major VP7 (G) and VP4 (P) genotype combinations, comprising G1P[8], G2P[4], G3P[8], G4P[8] and G9P[8]. However, G8, a common bovine rotavirus genotype, has been reported frequently among children in African countries. Surveillance of rotavirus gastroenteritis conducted in a sentinel hospital in Blantyre, Malawi between 1997 and 2007 provided a rare opportunity to examine the whole genotype constellation of G8 strains and their evolution over time. A sample of 27 (9.0 %) of 299 G8 strains was selected to represent each surveillance year and a range of P genotypes, which shifted in predominance from P[6] to P[4] and P[8] during the study period. Following cell culture adaptation, whole genome sequencing demonstrated that the genetic background of 26 strains possessed the DS-1 genotype constellation. A single G8P[6] strain was a reassortant in which both NSP2 and NSP5 genes from strains with the Wa genotype constellation had been inserted into a strain with the DS-1 genotype background. Phylogenetic analysis suggested frequent reassortment among co-circulating strains with the DS-1 genotype constellation. Little evidence was identified to suggest the introduction of contemporary bovine rotavirus genes into any of the 27 G8 strains examined. In conclusion, Malawian G8 strains are closely related to other human strains with the DS-1 genotype constellation. They have evolved over the last decade through genetic reassortment with other human rotaviruses, changing their VP4 genotypes while maintaining a conserved genotype constellation for the remaining structural and non-structural proteins.

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.050625-0
2013-06-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/6/1273.html?itemId=/content/journal/jgv/10.1099/vir.0.050625-0&mimeType=html&fmt=ahah

References

  1. Adah M. I., Nagashima S., Wakuda M., Taniguchi K. 2003; Close relationship between G8-serotype bovine and human rotaviruses isolated in Nigeria. J Clin Microbiol 41:3945–3950 [View Article][PubMed]
     [Google Scholar]
  2. Alkan F., Ozkul A., Oguzoglu T. C., Timurkan M. O., Caliskan E., Martella V., Burgu I. 2010; Distribution of G (VP7) and P (VP4) genotypes of group A bovine rotaviruses from Turkish calves with diarrhea, 1997-2008. Vet Microbiol 141:231–237 [View Article][PubMed]
     [Google Scholar]
  3. Bányai K., Martella V., Molnár P., Mihály I., Van Ranst M., Matthijnssens J. 2009; Genetic heterogeneity in human G6P[14] rotavirus strains detected in Hungary suggests independent zoonotic origin. J Infect 59:213–215 [View Article][PubMed]
     [Google Scholar]
  4. Bányai K., Papp H., Dandár E., Molnár P., Mihály I., Van Ranst M., Martella V., Matthijnssens J. 2010; Whole genome sequencing and phylogenetic analysis of a zoonotic human G8P[14] rotavirus strain. Infect Genet Evol 10:1140–1144 [View Article][PubMed]
     [Google Scholar]
  5. Bányai K., Mijatovic-Rustempasic S., Hull J. J., Esona M. D., Freeman M. M., Frace A. M., Bowen M. D., Gentsch J. R. 2011; Sequencing and phylogenetic analysis of the coding region of six common rotavirus strains: evidence for intragenogroup reassortment among co-circulating G1P[8] and G2P[4] strains from the United States. J Med Virol 83:532–539 [View Article][PubMed]
     [Google Scholar]
  6. Bányai K., László B., Duque J., Steele A. D., Nelson E. A., Gentsch J. R., Parashar U. D. 2012; Systematic review of regional and temporal trends in global rotavirus strain diversity in the pre rotavirus vaccine era: insights for understanding the impact of rotavirus vaccination programs. Vaccine 30:Suppl 1A122–A130 [View Article][PubMed]
     [Google Scholar]
  7. Chen Y., Wen Y., Liu X., Xiong X., Cao Z., Zhao Q., Yu Y., Yin X., Li C., Fan Y. 2008; Full genomic analysis of human rotavirus strain TB-Chen isolated in China. Virology 375:361–373 [View Article][PubMed]
     [Google Scholar]
  8. Cunliffe N. A., Gondwe J. S., Broadhead R. L., Molyneux M. E., Woods P. A., Bresee J. S., Glass R. I., Gentsch J. R., Hart C. A. 1999; Rotavirus G and P types in children with acute diarrhea in Blantyre, Malawi, from 1997 to 1998: predominance of novel P[6]G8 strains. J Med Virol 57:308–312 [View Article][PubMed]
     [Google Scholar]
  9. Cunliffe N. A., Gentsch J. R., Kirkwood C. D., Gondwe J. S., Dove W., Nakagomi O., Nakagomi T., Hoshino Y., Bresee J. S. other authors 2000; Molecular and serologic characterization of novel serotype G8 human rotavirus strains detected in Blantyre, Malawi. Virology 274:309–320 [View Article][PubMed]
     [Google Scholar]
  10. Cunliffe N. A., Gondwe J. S., Graham S. M., Thindwa B. D., Dove W., Broadhead R. L., Molyneux M. E., Hart C. A. 2001; Rotavirus strain diversity in Blantyre, Malawi, from 1997 to 1999. J Clin Microbiol 39:836–843 [View Article][PubMed]
     [Google Scholar]
  11. Cunliffe N. A., Ngwira B. M., Dove W., Thindwa B. D., Turner A. M., Broadhead R. L., Molyneux M. E., Hart C. A. 2010; Epidemiology of rotavirus infection in children in Blantyre, Malawi, 1997-2007. J Infect Dis 202:SupplS168–S174 [View Article][PubMed]
     [Google Scholar]
  12. De Grazia S., Giammanco G. M., Potgieter C. A., Matthijnssens J., Banyai K., Platia M. A., Colomba C., Martella V. 2010; Unusual assortment of segments in 2 rare human rotavirus genomes. Emerg Infect Dis 16:859–862 [View Article][PubMed]
     [Google Scholar]
  13. Desselberger U., Huppertz H. I. 2011; Immune responses to rotavirus infection and vaccination and associated correlates of protection. J Infect Dis 203:188–195 [View Article][PubMed]
     [Google Scholar]
  14. Doan Y. H., Nakagomi T., Nakagomi O. 2012; Repeated circulation over 6 years of intergenogroup mono-reassortant G2P[4] rotavirus strains with genotype N1 of the NSP2 gene. Infect Genet Evol 12:1202–1212 [View Article][PubMed]
     [Google Scholar]
  15. Doan Y. H., Nakagomi T., Aboudy Y., Silberstein I., Behar-Novat E., Nakagomi O., Shulman L. M. 2013; Identification by full-genome analysis of a bovine rotavirus transmitted directly to and causing diarrhea in a human child. J Clin Microbiol 51:182–189 [View Article][PubMed]
     [Google Scholar]
  16. Franco M. A., Angel J., Greenberg H. B. 2006; Immunity and correlates of protection for rotavirus vaccines. Vaccine 24:2718–2731 [View Article][PubMed]
     [Google Scholar]
  17. Ghosh S., Alam M. M., Ahmed M. U., Talukdar R. I., Paul S. K., Kobayashi N. 2010; Complete genome constellation of a caprine group A rotavirus strain reveals common evolution with ruminant and human rotavirus strains. J Gen Virol 91:2367–2373 [View Article][PubMed]
     [Google Scholar]
  18. Ghosh S., Paul S. K., Hossain M. A., Alam M. M., Ahmed M. U., Kobayashi N. 2011a; Full genomic analyses of two human G2P[4] rotavirus strains detected in 2005: identification of a caprine-like VP3 gene. J Gen Virol 92:1222–1227 [View Article][PubMed]
     [Google Scholar]
  19. Ghosh S., Adachi N., Gatheru Z., Nyangao J., Yamamoto D., Ishino M., Urushibara N., Kobayashi N. 2011b; Whole-genome analysis reveals the complex evolutionary dynamics of Kenyan G2P[4] human rotavirus strains. J Gen Virol 92:2201–2208 [View Article][PubMed]
     [Google Scholar]
  20. Ghosh S., Gatheru Z., Nyangao J., Adachi N., Urushibara N., Kobayashi N. 2011c; Full genomic analysis of a G8P[1] rotavirus strain isolated from an asymptomatic infant in Kenya provides evidence for an artiodactyl-to-human interspecies transmission event. J Med Virol 83:367–376 [View Article][PubMed]
     [Google Scholar]
  21. Heiman E. M., McDonald S. M., Barro M., Taraporewala Z. F., Bar-Magen T., Patton J. T. 2008; Group A human rotavirus genomics: evidence that gene constellations are influenced by viral protein interactions. J Virol 82:11106–11116 [View Article][PubMed]
     [Google Scholar]
  22. 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 [View Article][PubMed]
     [Google Scholar]
  23. Jere K. C., Mlera L., O’Neill H. G., Potgieter A. C., Page N. A., Seheri M. L., van Dijk A. A. 2011; Whole genome analyses of African G2, G8, G9, and G12 rotavirus strains using sequence-independent amplification and 454® pyrosequencing. J Med Virol 83:2018–2042 [View Article][PubMed]
     [Google Scholar]
  24. Jere K. C., Mlera L., O’Neill H. G., Peenze I., van Dijk A. A. 2012; Whole genome sequence analyses of three African bovine rotaviruses reveal that they emerged through multiple reassortment events between rotaviruses from different mammalian species. Vet Microbiol 159:245–250 [View Article][PubMed]
     [Google Scholar]
  25. Kutsuzawa T., Konno T., Suzuki H., Kapikian A. Z., Ebina T., Ishida N. 1982; Isolation of human rotavirus subgroups 1 and 2 in cell culture. J Clin Microbiol 16:727–730[PubMed]
     [Google Scholar]
  26. Maes P., Matthijnssens J., Rahman M., Van Ranst M. 2009; RotaC: a web-based tool for the complete genome classification of group A rotaviruses. BMC Microbiol 9:238 [View Article][PubMed]
     [Google Scholar]
  27. Matsuno S., Hasegawa A., Mukoyama A., Inouye S. 1985; A candidate for a new serotype of human rotavirus. J Virol 54:623–624[PubMed]
     [Google Scholar]
  28. Matthijnssens J., Rahman M., Yang X., Delbeke T., Arijs I., Kabue J. P., Muyembe J. J., Van Ranst M. 2006; G8 rotavirus strains isolated in the Democratic Republic of Congo belong to the DS-1-like genogroup. J Clin Microbiol 44:1801–1809 [View Article][PubMed]
     [Google Scholar]
  29. Matthijnssens J., Ciarlet M., Heiman E., Arijs I., Delbeke T., McDonald S. M., Palombo E. A., Iturriza-Gómara M., Maes P. other authors 2008a; Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 82:3204–3219 [View Article][PubMed]
     [Google Scholar]
  30. Matthijnssens J., Rahman M., Van Ranst M. 2008b; Two out of the 11 genes of an unusual human G6P[6] rotavirus isolate are of bovine origin. J Gen Virol 89:2630–2635 [View Article][PubMed]
     [Google Scholar]
  31. Matthijnssens J., Potgieter C. A., Ciarlet M., Parreño V., Martella V., Bányai K., Garaicoechea L., Palombo E. A., Novo L. other authors 2009; Are human P[14] rotavirus strains the result of interspecies transmissions from sheep or other ungulates that belong to the mammalian order Artiodactyla?. J Virol 83:2917–2929 [View Article][PubMed]
     [Google Scholar]
  32. Matthijnssens J., Taraporewala Z. F., Yang H., Rao S., Yuan L., Cao D., Hoshino Y., Mertens P. P., Carner G. R. other authors 2010; Simian rotaviruses possess divergent gene constellations that originated from interspecies transmission and reassortment. J Virol 84:2013–2026 [View Article][PubMed]
     [Google Scholar]
  33. Matthijnssens J., Ciarlet M., McDonald S. M., Attoui H., Bányai K., Brister J. R., Buesa J., Esona M. D., Estes M. K. other authors 2011; Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 156:1397–1413 [View Article][PubMed]
     [Google Scholar]
  34. McDonald S. M., McKell A. O., Rippinger C. M., McAllen J. K., Akopov A., Kirkness E. F., Payne D. C., Edwards K. M., Chappell J. D., Patton J. T. 2012; Diversity and relationships of cocirculating modern human rotaviruses revealed using large-scale comparative genomics. J Virol 86:9148–9162 [View Article][PubMed]
     [Google Scholar]
  35. Midgley S. E. K., Bányai K., Buesa J., Halaihel N., Hjulsager C. K., Jakab F., Kaplon J., Larsen L. E., Monini M. other authors 2012; Diversity and zoonotic potential of rotaviruses in swine and cattle across Europe. Vet Microbiol 156:238–245 [View Article][PubMed]
     [Google Scholar]
  36. Monini M., Cappuccini F., Battista P., Falcone E., Lavazza A., Ruggeri F. M. 2008; Molecular characterization of bovine rotavirus strains circulating in northern Italy, 2003-2005. Vet Microbiol 129:384–389 [View Article][PubMed]
     [Google Scholar]
  37. Mukherjee A., Ghosh S., Bagchi P., Dutta D., Chattopadhyay S., Kobayashi N., Chawla-Sarkar M. 2011; Full genomic analyses of human rotavirus G4P[4], G4P[6], G9P[19] and G10P[6] strains from North-eastern India: evidence for interspecies transmission and complex reassortment events. Clin Microbiol Infect 17:1343–1346[PubMed] [CrossRef]
     [Google Scholar]
  38. Naghipour M., Nakagomi T., Nakagomi O. 2008; Issues with reducing the rotavirus-associated mortality by vaccination in developing countries. Vaccine 26:3236–3241 [View Article][PubMed]
     [Google Scholar]
  39. Page N., Esona M., Seheri M., Nyangao J., Bos P., Mwenda J., Steele D. 2010; Characterization of genotype G8 strains from Malawi, Kenya, and South Africa. J Med Virol 82:2073–2081 [View Article][PubMed]
     [Google Scholar]
  40. Parashar U. D., Burton A., Lanata C., Boschi-Pinto C., Shibuya K., Steele D., Birmingham M., Glass R. I. 2009; Global mortality associated with rotavirus disease among children in 2004. J Infect Dis 200:Suppl 1S9–S15 [View Article][PubMed]
     [Google Scholar]
  41. Pietsch C., Petersen L., Patzer L., Liebert U. G. 2009; Molecular characteristics of German G8P[4] rotavirus strain GER1H-09 suggest that a genotyping and subclassification update is required for G8. J Clin Microbiol 47:3569–3576 [View Article][PubMed]
     [Google Scholar]
  42. Rahman M., Matthijnssens J., Yang X., Delbeke T., Arijs I., Taniguchi K., Iturriza-Gómara M., Iftekharuddin N., Azim T., Van Ranst M. 2007; Evolutionary history and global spread of the emerging g12 human rotaviruses. J Virol 81:2382–2390 [View Article][PubMed]
     [Google Scholar]
  43. Suzuki Y., Sanekata T., Sato M., Tajima K., Matsuda Y., Nakagomi O. 1993; Relative frequencies of G (VP7) and P (VP4) serotypes determined by polymerase chain reaction assays among Japanese bovine rotaviruses isolated in cell culture. J Clin Microbiol 31:3046–3049[PubMed]
     [Google Scholar]
  44. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
     [Google Scholar]
  45. Tate J. E., Patel M. M., Steele A. D., Gentsch J. R., Payne D. C., Cortese M. M., Nakagomi O., Cunliffe N. A., Jiang B. other authors 2010; Global impact of rotavirus vaccines. Expert Rev Vaccines 9:395–407 [View Article][PubMed]
     [Google Scholar]
  46. Tate J. E., Burton A. H., Boschi-Pinto C., Steele A. D., Duque J., Parashar U. D. WHO-coordinated Global Rotavirus Surveillance Network 2012; 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis 12:136–141 [View Article][PubMed]
     [Google Scholar]
  47. Todd S., Page N. A., Duncan Steele A., Peenze I., Cunliffe N. A. 2010; Rotavirus strain types circulating in Africa: Review of studies published during 1997-2006. J Infect Dis 202:SupplS34–S42 [View Article][PubMed]
     [Google Scholar]
  48. World Health Organization 2009; Meeting of the immunization Strategic Advisory Group of Experts, April 2009 – conclusions and recommendations. Wkly Epidemiol Rec 84:220–236[PubMed]
     [Google Scholar]
  49. Xie J. X., Duan Z. J., Li D. D., Li B. W., Lan B., Li Y. Q., Kong X. Y., Zhang Q., Li J. 2010; [Detection of bovine rotavirus G10P[11] in a dairy farm in Daqing, China]. Bing Du Xue Bao 26:407–409 (In Chinese) [PubMed]
     [Google Scholar]
  50. Zeller M., Heylen E., De Coster S., Van Ranst M., Matthijnssens J. 2012; Full genome characterization of a porcine-like human G9P[6] rotavirus strain isolated from an infant in Belgium. Infect Genet Evol 12:1492–1500 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.050625-0
Loading
G8 rotaviruses with conserved genotype constellations detected in Malawi over 10 years (1997–2007) display frequent gene reassortment among strains co-circulating in humans
J. Gen. Virol. 94, 1273 (2013); https://doi.org/10.1099/vir.0.050625-0
/content/journal/jgv/10.1099/vir.0.050625-0
/content/journal/jgv/10.1099/vir.0.050625-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited 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