1887

Journal of General Virology header logo

Volume 102, Issue 3

The origins of G12P[6] rotavirus strains detected in Lebanon Free

Abstract

The G12 rotaviruses are an increasingly important cause of severe diarrhoea in infants and young children worldwide. Seven human G12P[6] rotavirus strains were detected in stool samples from children hospitalized with gastroenteritis in Lebanon during a 2011–2013 surveillance study. Complete genomes of these strains were sequenced using VirCapSeq-VERT, a capture-based high-throughput viral-sequencing method, and further characterized based on phylogenetic analyses with global RVA and vaccine strains. Based on the complete genomic analysis, all Lebanese G12 strains were found to have Wa-like genetic backbone G12-P[6]-I1-R1-C1-M1-A1-N1-T1-E1-H1. Phylogenetically, these strains fell into two clusters where one of them might have emerged from Southeast Asian strains and the second one seems to have a mixed backbone between North American and Southeast Asian strains. Further analysis of these strains revealed high antigenic variability compared to available vaccine strains. To our knowledge, this is the first report on the complete genome-based characterization of G12P[6] emerging in Lebanon. Additional studies will provide important insights into the evolutionary dynamics of G12 rotaviruses spreading in Asia.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): G12P[6] , Genome , Human Rotavirus A , Lebanon and VirCapSeq-VERT
Funding
This study was supported by the:
  • Foundation for the National Institutes of Health (Award U19AI109761)
    • Principle Award Recipient: W.Ian Lipkin
© 2021 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001535
2020-12-17
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/102/3/vir001535.html?itemId=/content/journal/jgv/10.1099/jgv.0.001535&mimeType=html&fmt=ahah

References

  1. Troeger C, Khalil IA, Rao PC, Cao S, Blacker BF et al. Rotavirus vaccination and the global burden of rotavirus diarrhea among children younger than 5 years. JAMA Pediatr 2018; 172:958–965 [View Article][PubMed]
     [Google Scholar]
  2. Dbaibo G, Rajab M, Inati A, Mikhael R, Choueiry E et al. Hospital-Based surveillance study of rotavirus gastroenteritis in children under 5 years of age in Lebanon. Trials in Vaccinology 2013; 2:Pages 25–30
     [Google Scholar]
  3. Crawford SE, Ramani S, Tate JE, Parashar UD, Svensson L et al. Rotavirus infection. Nat Rev Dis Primers 2017; 3:17083 [View Article][PubMed]
     [Google Scholar]
  4. Matthijnssens J, Bilcke J, Ciarlet M, Martella V, Bányai K et al. Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol 2009; 4:1303–1316 [View Article][PubMed]
     [Google Scholar]
  5. Jere KC, Mlera L, O'Neill HG, Potgieter AC, Page NA et al. Whole genome analyses of African G2, G8, G9, and G12 rotavirus strains using sequence-independent amplification and 454® pyrosequencing. J Med Virol 2011; 83:2018–2042 [View Article][PubMed]
     [Google Scholar]
  6. Bwogi J, Jere KC, Karamagi C, Byarugaba DK, Namuwulya P et al. Whole genome analysis of selected human and animal rotaviruses identified in Uganda from 2012 to 2014 reveals complex genome reassortment events between human, bovine, caprine and porcine strains. PLoS One 2017; 12:e0178855 [View Article][PubMed]
     [Google Scholar]
  7. Gentsch JR, Laird AR, Bielfelt B, Griffin DD, Banyai K et al. Serotype diversity and reassortment between human and animal rotavirus strains: implications for rotavirus vaccine programs. J Infect Dis 2005; 192 Suppl 1:S146–159 [View Article][PubMed]
     [Google Scholar]
  8. Matthijnssens J, Heylen E, Zeller M, Rahman M, Lemey P et al. Phylodynamic analyses of rotavirus genotypes G9 and G12 underscore their potential for swift global spread. Mol Biol Evol 2010; 27:2431–2436 [View Article][PubMed]
     [Google Scholar]
  9. Rahman M, Matthijnssens J, Yang X, Delbeke T, Arijs I et al. Evolutionary history and global spread of the emerging G12 human rotaviruses. J Virol 2007; 81:2382–2390 [View Article][PubMed]
     [Google Scholar]
  10. Aly M, Al Khairy A, Al Johani S, Balkhy H. Unusual rotavirus genotypes among children with acute diarrhea in Saudi Arabia. BMC Infect Dis 2015; 15:192 [View Article][PubMed]
     [Google Scholar]
  11. Kirby A, Al-Eryani A, Al-Sonboli N, Hafiz T, Beyer M et al. Rotavirus and norovirus infections in children in Sana'a, Yemen. Trop Med Int Health 2011; 16:680–684 [View Article][PubMed]
     [Google Scholar]
  12. Ahmed S, Klena J, Albana A, Alhamdani F, Oskoff J et al. Characterization of human rotaviruses circulating in Iraq in 2008: atypical G8 and high prevalence of P[6] strains. Infect Genet Evol 2013; 16:212–217 [View Article][PubMed]
     [Google Scholar]
  13. Azaran A, Makvandi M, Teimoori A, Ebrahimi S, Heydari F et al. Distribution of rotavirus genotypes Ccirculating in Ahvaz, Iran in 2016. Iran Biomed J 2018; 22:107–116 [View Article][PubMed]
     [Google Scholar]
  14. Moussa A, Ben Hadj Fredj M, Fodha I, BenHamida-Rebaï M, Kacem S et al. Distribution of rotavirus VP7 and VP4 genotypes circulating in Tunisia from 2009 to 2014: emergence of the genotype G12. J Med Microbiol 2016; 65:1028–1037 [View Article][PubMed]
     [Google Scholar]
  15. Moussa A, Fredj MBH, BenHamida-Rebaï M, Fodha I, Boujaafar N et al. Phylogenetic analysis of partial VP7 gene of the emerging human group A rotavirus G12 strains circulating in Tunisia. J Med Microbiol 2017; 66:112–118 [View Article][PubMed]
     [Google Scholar]
  16. Kamel AH, Ali MA, El-Nady HG, de Rougemont A, Pothier P et al. Predominance and circulation of enteric viruses in the region of greater Cairo, Egypt. J Clin Microbiol 2009; 47:1037–1045 [View Article][PubMed]
     [Google Scholar]
  17. Alam MM, Malik SA, Shaukat S, Naeem A, Sharif S et al. Genetic characterization of rotavirus subtypes in Pakistan-first report of G12 genotype from Pakistan under WHO-Eastern Mediterranean region. Virus Res 2009; 144:280–284 [View Article][PubMed]
     [Google Scholar]
  18. Aydin H, Aktaş O, Aktas O. Rotavirus genotypes in children with gastroenteritis in Erzurum: first detection of G12P[6] and G12P[8] genotypes in Turkey. Prz Gastroenterol 2017; 12:122–127 [View Article][PubMed]
     [Google Scholar]
  19. Matthijnssens J, Van Ranst M. Genotype constellation and evolution of group A rotaviruses infecting humans. Curr Opin Virol 2012; 2:426–433 [View Article][PubMed]
     [Google Scholar]
  20. Jere KC, Chaguza C, Bar-Zeev N, Lowe J, Peno C et al. Emergence of Double- and Triple-Gene Reassortant G1P[8] Rotaviruses Possessing a DS-1-Like Backbone after Rotavirus Vaccine Introduction in Malawi. J Virol 2018; 92: 01 02 2018 [View Article][PubMed]
     [Google Scholar]
  21. Ali Z, Harastani H, Hammadi M, Reslan L, Ghanem S et al. Rotavirus genotypes and vaccine effectiveness from a sentinel, hospital-based, surveillance study for three consecutive rotavirus seasons in Lebanon. PLoS One 2016; 11:e0161345 [View Article][PubMed]
     [Google Scholar]
  22. Lewis K. Vesikari clinical severity scoring manual. PATH 2011
     [Google Scholar]
  23. Mishra N, Reslan L, El-Husseini M, Raoof H, Finianos M et al. Full genome characterization of human G3P[6] and G3P[9] rotavirus strains in Lebanon. Infect Genet Evol 2020; 78:104133 [View Article][PubMed]
     [Google Scholar]
  24. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article][PubMed]
     [Google Scholar]
  25. Aoki ST, Settembre EC, Trask SD, Greenberg HB, Harrison SC et al. Structure of rotavirus outer-layer protein VP7 bound with a neutralizing Fab. Science 2009; 324:1444–1447 [View Article][PubMed]
     [Google Scholar]
  26. Dormitzer PR, Nason EB, Prasad BVV, Harrison SC. Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 2004; 430:1053–1058 [View Article][PubMed]
     [Google Scholar]
  27. Dormitzer PR, Sun Z-YJ, Wagner G, Harrison SC. The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. Embo J 2002; 21:885–897 [View Article][PubMed]
     [Google Scholar]
  28. Estes M, Kapikian AZR, Knipe IDM, Howley PM, Griffin RA et al. Fields virology 2, 5th ed. Philadelphia: Lippincott Williams Wolters Kluwer; 2007 pp 1917–1974
     [Google Scholar]
  29. Gilbert JM, Greenberg HB. Cleavage of rhesus rotavirus VP4 after arginine 247 is essential for rotavirus-like particle-induced fusion from without. J Virol 1998; 72:5323–5327 [View Article][PubMed]
     [Google Scholar]
  30. Arias CF, Romero P, Alvarez V, López S. Trypsin activation pathway of rotavirus infectivity. J Virol 1996; 70:5832–5839 [View Article][PubMed]
     [Google Scholar]
  31. Crawford SE, Mukherjee SK, Estes MK, Lawton JA, Shaw AL et al. Trypsin cleavage stabilizes the rotavirus VP4 spike. J Virol 2001; 75:6052–6061 [View Article][PubMed]
     [Google Scholar]
  32. Vizzi E, Piñeros OA, Oropeza MD, Naranjo L, Suárez JA et al. Human rotavirus strains circulating in Venezuela after vaccine introduction: predominance of G2P[4] and reemergence of G1P[8]. Virol J 2017; 14:58 [View Article][PubMed]
     [Google Scholar]
  33. Ogden KM, Tan Y, Akopov A, Stewart LS, McHenry R et al. Multiple Introductions and Antigenic Mismatch with Vaccines May Contribute to Increased Predominance of G12P[8] Rotaviruses in the United States. J Virol 2019; 93: 01 01 2019 [View Article][PubMed]
     [Google Scholar]
  34. Ciarlet M, Hyser JM, Estes MK. Sequence analysis of the VP4, VP6, VP7, and NSP4 gene products of the bovine rotavirus WC3. Virus Genes 2002; 24:107–118 [View Article][PubMed]
     [Google Scholar]
  35. Stirzaker SC, Whitfeld PL, Christie DL, Bellamy AR, Both GW. Processing of rotavirus glycoprotein VP7: implications for the retention of the protein in the endoplasmic reticulum. J Cell Biol 1987; 105:2897–2903 [View Article][PubMed]
     [Google Scholar]
  36. Mirazimi A, Svensson L. Carbohydrates facilitate correct disulfide bond formation and folding of rotavirus VP7. J Virol 1998; 72:3887–3892 [View Article][PubMed]
     [Google Scholar]
  37. Nakagomi T, Do LP, Agbemabiese CA, Kaneko M, Gauchan P et al. Whole-genome characterisation of G12P[6] rotavirus strains possessing two distinct genotype constellations co-circulating in Blantyre, Malawi, 2008. Arch Virol 2017; 162:213–226 [View Article][PubMed]
     [Google Scholar]
  38. Motayo BO, Oluwasemowo OO, Olusola BA, Opayele AV, Faneye AO. Phylogeography and evolutionary analysis of African rotavirus a genotype G12 reveals district genetic diversification within lineage III. Heliyon 2019; 5:e02680 [View Article][PubMed]
     [Google Scholar]
  39. Bányai K, László B, Duque J, Steele AD, Nelson EAS et al. 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 2012; 30 Suppl 1:A122–130 [View Article][PubMed]
     [Google Scholar]
  40. Taniguchi K, Urasawa T, Kobayashi N, Gorziglia M, Urasawa S. Nucleotide sequence of VP4 and VP7 genes of human rotaviruses with subgroup I specificity and long RNA pattern: implication for new G serotype specificity. J Virol 1990; 64:5640–5644 [View Article][PubMed]
     [Google Scholar]
  41. Wylie KM, Stanley KM, TeKippe EM, Mihindukulasuriya K, Storch GA. Resurgence of rotavirus genotype G12 in St. Louis during the 2014-2015 rotavirus season. J Pediatric Infect Dis Soc 2017; 6:346–351 [View Article][PubMed]
     [Google Scholar]
  42. Castello AA, Argüelles MH, Rota RP, Olthoff A, Jiang B et al. Molecular epidemiology of group A rotavirus diarrhea among children in Buenos Aires, Argentina, from 1999 to 2003 and emergence of the infrequent genotype G12. J Clin Microbiol 2006; 44:2046–2050 [View Article][PubMed]
     [Google Scholar]
  43. Pun SB, Nakagomi T, Sherchand JB, Pandey BD, Cuevas LE et al. Detection of G12 human rotaviruses in Nepal. Emerg Infect Dis 2007; 13:482–484 [View Article][PubMed]
     [Google Scholar]
  44. Sherchand JB, Nakagomi O, Dove W, Nakagomi T, Yokoo M et al. Molecular epidemiology of rotavirus diarrhea among children aged <5 years in nepal: predominance of emergent G12 strains during 2 years. J Infect Dis 2009; 200 Suppl 1:S182–187 [View Article][PubMed]
     [Google Scholar]
  45. Khananurak K, Vutithanachot V, Simakachorn N, Theamboonlers A, Chongsrisawat V et al. Prevalence and phylogenetic analysis of rotavirus genotypes in Thailand between 2007 and 2009. Infect Genet Evol 2010; 10:537–545 [View Article][PubMed]
     [Google Scholar]
  46. Kang G, Desai R, Arora R, Chitamabar S, Naik TN et al. Diversity of circulating rotavirus strains in children hospitalized with diarrhea in India, 2005-2009. Vaccine 2013; 31:2879–2883 [View Article][PubMed]
     [Google Scholar]
  47. Mukherjee A, Chattopadhyay S, Bagchi P, Dutta D, Singh NB et al. Surveillance and molecular characterization of rotavirus strains circulating in Manipur, north-eastern India: increasing prevalence of emerging G12 strains. Infect Genet Evol 2010; 10:311–320 [View Article][PubMed]
     [Google Scholar]
  48. Rahman M, Sultana R, Ahmed G, Nahar S, Hassan ZM et al. Prevalence of G2P[4] and G12P[6] rotavirus, Bangladesh. Emerg Infect Dis 2007; 13:18–24 [View Article][PubMed]
     [Google Scholar]
  49. Tra My PV, Rabaa MA, Vinh H, Holmes EC, Hoang NVM et al. The emergence of rotavirus G12 and the prevalence of enteric viruses in hospitalized pediatric diarrheal patients in southern Vietnam. Am J Trop Med Hyg 2011; 85:768–775 [View Article][PubMed]
     [Google Scholar]
  50. Le VP, Kim J-Y, Cho S-L, Nam S-W, Lim I et al. Detection of unusual rotavirus genotypes G8P[8] and G12P[6] in South Korea. J Med Virol 2008; 80:175–182 [View Article][PubMed]
     [Google Scholar]
  51. Ide T, Komoto S, Higo-Moriguchi K, Htun KW, Myint YY et al. Whole Genomic Analysis of Human G12P[6] and G12P[8] Rotavirus Strains that Have Emerged in Myanmar. PLoS One 2015; 10:e0124965 [View Article][PubMed]
     [Google Scholar]
  52. Cilla G, Montes M, Gomariz M, Alkorta M, Iturzaeta A et al. Rotavirus genotypes in children in the Basque Country (North of Spain): rapid and intense emergence of the G12[P8] genotype. Epidemiol Infect 2013; 141:868–874 [View Article][PubMed]
     [Google Scholar]
  53. Boni-Cisse C, Meite S, Mlan AB, Zaba F, N'Guessan R et al. Genotypic characterization of rotavirus in children under 5 years circulating in Côte d'Ivoire from 2010 to 2013. Virol J 2018; 15:78 [View Article][PubMed]
     [Google Scholar]
  54. Umair M, Salman M, Alam MM, Rana MS, Zaidi SSZ et al. Rotavirus surveillance in Pakistan during 2015-2016 reveals high prevalence of G12P[6]. J Med Virol 2018; 90:1272–1276 [View Article][PubMed]
     [Google Scholar]
  55. Clarke E, Desselberger U. Correlates of protection against human rotavirus disease and the factors influencing protection in low-income settings. Mucosal Immunol 2015; 8:1–17 [View Article][PubMed]
     [Google Scholar]
  56. Greenberg HB, Estes MK. Rotaviruses: from pathogenesis to vaccination. Gastroenterology 2009; 136:1939–1951 [View Article][PubMed]
     [Google Scholar]
  57. Sharma S, Nakagomi T, Nakagomi O, Paul VK, Bhan MK et al. Convalescent phase sera from children infected with G12 rotavirus cross-neutralize rotavirus strains belonging to the WA genogroup. J Gen Virol 2010; 91:1794–1799 [View Article][PubMed]
     [Google Scholar]
  58. Payne DC, Baggs J, Klein NP, Parashar UD. Does preventing rotavirus infections through vaccination also protect against naturally occurring intussusception over time?. Clin Infect Dis 2015; 60:163–164 [View Article][PubMed]
     [Google Scholar]
  59. Burns JW, Siadat-Pajouh M, Krishnaney AA, Greenberg HB. Protective effect of rotavirus VP6-specific IgA monoclonal antibodies that lack neutralizing activity. Science 1996; 272:104–107 [View Article][PubMed]
     [Google Scholar]
  60. Ward RL. Rotavirus vaccines: how they work or don't work. Expert Rev Mol Med 2008; 10:e5 [View Article][PubMed]
     [Google Scholar]
  61. Parra M, Herrera D, Jácome MF, Mesa MC, Rodríguez L-S et al. Circulating rotavirus-specific T cells have a poor functional profile. Virology 2014; 468-470:340–350 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001535
Loading
The origins of G12P[6] rotavirus strains detected in Lebanon
J. Gen. Virol. 102, 001535 (2021); https://doi.org/10.1099/jgv.0.001535
/content/journal/jgv/10.1099/jgv.0.001535
/content/journal/jgv/10.1099/jgv.0.001535
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

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