1887

Abstract

Group A rotavirus (RVA) is the leading cause of severe gastroenteritis in children younger than 5 years. The most common human G-types are G1-4 and G9. G12 genotype is currently emerging worldwide, becoming the sixth most prevalent RVA G-genotype. In Tunisia, an emergence of G12 RVA strains was observed. To understand the evolution and origin of these Tunisian G12 strains, phylogenetic analyses were conducted.

A total of 1127 faecal samples were collected from Tunisian children under 5 years consulting for gastroenteritis between 2009 and 2014. Samples were screened by ELISA for the presence of RVA antigen. RVA-positive samples were used for the detection of G12 RVA strains by semi-nested RT-PCR. G12-positive specimens were subjected to VP4 genotyping reaction. PCR products of the G12-positive samples were sequenced and characterized by phylogenetic analysis of partial VP7 gene sequence.

Globally, 270 (24 %) stool specimens were RVA-positive. Fourteen presented the G12 genotype (5.2 %) and were found to be in combination with either the P[6] (50.0 %) or the P[8] (50.0 %) genotype. Phylogenetic analysis revealed that all characterized Tunisian G12 strains clustered in the modern G12 lineage III and appear to form three different subclusters.

Thus, the Tunisian G12 strains may have originated from not a single, but at least three distinct ancestral G12 strains. Detailed molecular characterization of the entire genome of these strains remains essential to help determine the extent of genetic variation and the relatedness of Tunisian G12 RVA strains to G12 strains described worldwide.

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2017-02-01
2024-03-28
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References

  1. Martella V, Bányai K, Matthijnssens J, Buonavoglia C, Ciarlet M. Zoonotic aspects of rotaviruses. Vet Microbiol 2010; 140:246–255 [View Article][PubMed]
    [Google Scholar]
  2. Kahn G, Fitzwater S, Tate J, Kang G, Ganguly N et al. Epidemiology and prospects for prevention of rotavirus disease in India. Indian Pediatr 2012; 49:467–474[PubMed] [CrossRef]
    [Google Scholar]
  3. Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J et al. 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 2012; 12:136–141 [View Article][PubMed]
    [Google Scholar]
  4. Walker CL, Rudan I, Liu L, Nair H, Theodoratou E et al. Global burden of childhood pneumonia and diarrhoea. Lancet 2013; 381:1405–1416 [View Article][PubMed]
    [Google Scholar]
  5. Estes MK, Greenberg HB. Rotaviruses. In Knipe PM, Howley DM. (editors) Fields Virology, 6th ed. Philadelphia: Lippincott Williams & Wilkins; 2013 pp. 1347–1401
    [Google Scholar]
  6. Matthijnssens J, Otto PH, Ciarlet M, Desselberger U, van Ranst M et al. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol 2012; 157:1177–1182 [View Article][PubMed]
    [Google Scholar]
  7. Matthijnssens J, Ciarlet M, Mcdonald SM, Attoui H, Bányai K et al. Uniformity of rotavirus strain nomenclature proposed by the rotavirus classification working group (RCWG). Arch Virol 2011; 156:1397–1413 [View Article][PubMed]
    [Google Scholar]
  8. Trojnar E, Sachsenröder J, Twardziok S, Reetz J, Otto PH et al. Identification of an avian group A rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotaviruses. J Gen Virol 2013; 94:136–142 [View Article][PubMed]
    [Google Scholar]
  9. Bányai K, László B, Duque J, Steele AD, Nelson EA 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:A122–A130 [View Article][PubMed]
    [Google Scholar]
  10. Gómez MM, Resque HR, Volotão EM, Rose TL, da Silva MF et al. Distinct evolutionary origins of G12P[8] and G12P[9] group A rotavirus strains circulating in Brazil. Infect Genet Evol 2014; 28:385–388 [View Article][PubMed]
    [Google Scholar]
  11. 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]
  12. 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]
  13. Stupka JA, Degiuseppe JI, Parra GI. Argentinean National Rotavirus Surveillance Network Increased frequency of rotavirus G3P[8] and G12P[8] in Argentina during 2008-2009: whole-genome characterization of emerging G12P[8] strains. J Clin Virol 2012; 54:162–167 [View Article][PubMed]
    [Google Scholar]
  14. 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[PubMed]
    [Google Scholar]
  15. Das S, Varghese V, Chaudhury S, Barman P, Mahapatra S et al. Emergence of novel human group A rotavirus G12 strains in India. J Clin Microbiol 2003; 41:2760–2762[PubMed] [CrossRef]
    [Google Scholar]
  16. Griffin DD, Nakagomi T, Hoshino Y, Nakagomi O, Kirkwood CD et al. Characterization of nontypeable rotavirus strains from the United States: identification of a new rotavirus reassortant (P2A[6],G12) and rare P3[9] strains related to bovine rotaviruses. Virology 2002; 294:256–269 [View Article][PubMed]
    [Google Scholar]
  17. Pongsuwanna Y, Guntapong R, Chiwakul M, Tacharoenmuang R, Onvimala N et al. Detection of a human rotavirus with G12 and P[9] specificity in Thailand. J Clin Microbiol 2002; 40:1390–1394[PubMed] [CrossRef]
    [Google Scholar]
  18. Samajdar S, Varghese V, Barman P, Ghosh S, Mitra U et al. Changing pattern of human group A rotaviruses: emergence of G12 as an important pathogen among children in eastern India. J Clin Virol 2006; 36:183–188 [View Article][PubMed]
    [Google Scholar]
  19. 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]
  20. Mwenda JM, Ntoto KM, Abebe A, Enweronu-Laryea C, Amina I et al. Burden and epidemiology of rotavirus diarrhea in selected African countries: preliminary results from the African rotavirus surveillance network. J Infect Dis 2010; 202:S5–S11 [View Article][PubMed]
    [Google Scholar]
  21. Seheri M, Nemarude L, Peenze I, Netshifhefhe L, Nyaga MM et al. Update of rotavirus strains circulating in Africa from 2007 through 2011. Pediatr Infect Dis J 2014; 33:S76–S84 [View Article][PubMed]
    [Google Scholar]
  22. Shinozaki K, Okada M, Nagashima S, Kaiho I, Taniguchi K. Characterization of human rotavirus strains with G12 and P[9] detected in Japan. J Med Virol 2004; 73:612–616 [View Article][PubMed]
    [Google Scholar]
  23. Wakuda M, Nagashima S, Kobayashi N, Pongsuwanna Y, Taniguchi K. Serologic and genomic characterization of a G12 human rotavirus in Thailand. J Clin Microbiol 2003; 41:5764–5769[PubMed] [CrossRef]
    [Google Scholar]
  24. Cunliffe NA, Ngwira BM, Dove W, Nakagomi O, Nakagomi T et al. Serotype G12 rotaviruses, Lilongwe, Malawi. Emerg Infect Dis 2009; 15:87–90 [View Article][PubMed]
    [Google Scholar]
  25. Enweronu-Laryea CC, Sagoe KW, Damanka S, Lartey B, Armah GE. Rotavirus genotypes associated with childhood severe acute diarrhoea in southern Ghana: a cross-sectional study. Virol J 2013; 10:287 [View Article][PubMed]
    [Google Scholar]
  26. Nakagomi T, Nakagomi O, Dove W, Doan YH, Witte D et al. Molecular characterization of rotavirus strains detected during a clinical trial of a human rotavirus vaccine in Blantyre, Malawi. Vaccine 2012; 30:A140–A151 [View Article][PubMed]
    [Google Scholar]
  27. Ndze VN, Papp H, Achidi EA, Gonsu KH, László B et al. One year survey of human rotavirus strains suggests the emergence of genotype G12 in Cameroon. J Med Virol 2013; 85:1485–1490 [View Article][PubMed]
    [Google Scholar]
  28. Oluwatoyin Japhet M, Adeyemi Adesina O, Famurewa O, Svensson L, Nordgren J. Molecular epidemiology of rotavirus and norovirus in Ile-Ife, Nigeria: high prevalence of G12P[8] rotavirus strains and detection of a rare norovirus genotype. J Med Virol 2012; 84:1489–1496 [View Article][PubMed]
    [Google Scholar]
  29. Page NA, de Beer MC, Seheri LM, Dewar JB, Steele AD. The detection and molecular characterization of human G12 genotypes in South Africa. J Med Virol 2009; 81:106–113 [View Article][PubMed]
    [Google Scholar]
  30. Page AL, Jusot V, Mamaty AA, Adamou L, Kaplon J et al. Rotavirus surveillance in urban and rural areas of Niger, April 2010-March 2012. Emerg Infect Dis 2014; 20:573–580 [View Article][PubMed]
    [Google Scholar]
  31. Pukuta ES, Esona MD, Nkongolo A, Seheri M, Makasi M et al. Molecular surveillance of rotavirus infection in the democratic republic of the Congo August 2009 to June 2012. Pediatr Infect Dis J 2014; 33:355–359 [View Article][PubMed]
    [Google Scholar]
  32. Mouna BH, Hamida-Rebaï MB, Heylen E, Zeller M, Moussa A et al. Sequence and phylogenetic analyses of human rotavirus strains: comparison of VP7 and VP8(∗) antigenic epitopes between Tunisian and vaccine strains before national rotavirus vaccine introduction. Infect Genet Evol 2013; 18:132–144 [View Article][PubMed]
    [Google Scholar]
  33. 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]
  34. Das BK, Gentsch JR, Cicirello HG, Woods PA, Gupta A et al. Characterization of rotavirus strains from newborns in New Delhi, India. J Clin Microbiol 1994; 32:1820–1822[PubMed]
    [Google Scholar]
  35. Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M et al. Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 1992; 30:1365–1373[PubMed]
    [Google Scholar]
  36. Simmonds MK, Armah G, Asmah R, Banerjee I, Damanka S et al. New oligonucleotide primers for P-typing of rotavirus strains: strategies for typing previously untypeable strains. J Clin Virol 2008; 42:368–373 [View Article][PubMed]
    [Google Scholar]
  37. Iturriza-Gómara M, Green J, Brown DW, Desselberger U, Gray JJ. Diversity within the VP4 gene of rotavirus P[8] strains: implications for reverse transcription-PCR genotyping. J Clin Microbiol 2000; 38:898–901[PubMed]
    [Google Scholar]
  38. Dugan KA, Lawrence HS, Hares DR, Fisher CL, Budowle B. An improved method for post-PCR purification for mtDNA sequence analysis. J Forensic Sci 2002; 47:811–818[PubMed] [CrossRef]
    [Google Scholar]
  39. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
    [Google Scholar]
  40. Iturriza Gómara M, Desselberger U, Gray J. Molecular epidemiology of rotaviruses: genetic mechanisms associated with diversity. In Desselberger U, Gray J. (editors) Viral gastroenteritis Amsterdam: Elsevier; 2003 pp. 317–344 [CrossRef]
    [Google Scholar]
  41. Santos N, Hoshino Y. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 2005; 15:29–56 [View Article][PubMed]
    [Google Scholar]
  42. 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:S146–S159 [View Article][PubMed]
    [Google Scholar]
  43. Bányai K, Bogdán A, Kisfali P, Molnár P, Mihály I et al. Emergence of serotype G12 rotaviruses, Hungary. Emerg Infect Dis 2007; 13:916–919 [View Article][PubMed]
    [Google Scholar]
  44. Kobayashi N, Lintag IC, Urasawa T, Taniguchi K, Saniel MC et al. Unusual human rotavirus strains having subgroup I specificity and ‘long’ RNA electropherotype. Arch Virol 1989; 109:11–23[PubMed] [CrossRef]
    [Google Scholar]
  45. Ghosh S, Varghese V, Samajdar S, Bhattacharya SK, Kobayashi N et al. Molecular characterization of a porcine group A rotavirus strain with G12 genotype specificity. Arch Virol 2006; 151:1329–1344 [View Article][PubMed]
    [Google Scholar]
  46. Ward RL, Bernstein DI. Rotarix: a rotavirus vaccine for the world. Clin Infect Dis 2009; 48:222–228 [View Article][PubMed]
    [Google Scholar]
  47. Ciarlet M, Schödel F. Development of a rotavirus vaccine: clinical safety, immunogenicity, and efficacy of the pentavalent rotavirus vaccine, RotaTeq. Vaccine 2009; 27:G72–G81 [View Article][PubMed]
    [Google Scholar]
  48. Matthijnssens J, Joelsson DB, Warakomski DJ, Zhou T, Mathis PK et al. Molecular and biological characterization of the 5 human-bovine rotavirus (WC3)-based reassortant strains of the pentavalent rotavirus vaccine, RotaTeq. Virology 2010; 403:111–127 [View Article][PubMed]
    [Google Scholar]
  49. Espejo PW, Peralta FO, Pacheres HC, del Valle LJ, Tapia AC et al. Diarrhoea caused by rotavirus in a regional Peruvian hospital: determination of circulating genotypes. Trans R Soc Trop Med Hyg 2014; 108:425–430 [View Article][PubMed]
    [Google Scholar]
  50. Neves MA, Pinheiro HH, Silva RS, Linhares AC, Silva LD et al. High prevalence of G12P[8] rotavirus strains in Rio Branco, Acre, Western Amazon, in the post-rotavirus vaccine introduction period. J Med Virol 2016; 88:782–789 [View Article][PubMed]
    [Google Scholar]
  51. Caillère N, Vilain P, Brottet E, Kaplon J, Ambert-Balay K et al. A major outbreak of gastroenteritis in Réunion Island in 2012: first identification of G12 rotavirus on the Island. Euro Surveill 2013; 18:20476[PubMed]
    [Google Scholar]
  52. Payne DC, Boom JA, Staat MA, Edwards KM, Szilagyi PG et al. Effectiveness of pentavalent and monovalent rotavirus vaccines in concurrent use among US children <5 years of age, 2009-2011. Clin Infect Dis 2013; 57:13–20 [View Article][PubMed]
    [Google Scholar]
  53. Steele AD, Neuzil KM, Cunliffe NA, Madhi SA, Bos P et al. Human rotavirus vaccine Rotarix™ provides protection against diverse circulating rotavirus strains in African infants: a randomized controlled trial. BMC Infect Dis 2012; 12:213 [View Article][PubMed]
    [Google Scholar]
  54. Freeman MM, Kerin T, Hull J, Teel E, Esona M et al. Phylogenetic analysis of novel G12 rotaviruses in the United States: a molecular search for the origin of a new strain. J Med Virol 2009; 81:736–746 [View Article][PubMed]
    [Google Scholar]
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