Large-scale whole genome sequencing identifies country-wide spread of an emerging G9P[8] rotavirus strain in Hungary, 2012

Infection, Genetics and Evolution

Volumn 28, Issue , 2014, Pages 495-512

  Dóró, Renáta ^a   Mihalov Kovács, Eszter ^a   Marton, Szilvia ^a   László, Brigitta ^b   Deák, Judit ^c   Jakab, Ferenc ^d   Juhász, Ágnes ^e   Kisfali, Péter ^d   Martella, Vito ^f   Melegh, Béla ^d   Molnár, Péter ^g   Sántha, Ildikó ^h   Schneider, Ferenc ⁱ   Bányai, Krisztián ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c UNIVERSITY OF SZEGED   (Hungary)

^d UNIVERSITY OF PÉCS   (Hungary)

^e Laboratory Ltd   (Hungary)

^f UNIVERSITY OF BARI   (Italy)

^g Szent Laszlo Hospital   (Hungary)

^h North Hungarian Regional Institute   (Hungary)

ⁱ Markusovszky Teaching Hospital   (Hungary)

Author keywords

Genotype; Rotavirus; Surveillance; Whole genome sequencing

Indexed keywords

ROTAVIRUS VACCINE; CAPSID PROTEIN;

ARTICLE; BOVINE LIKE VP1 GENE; CATTLE; CLONAL SPECIES; CONTROLLED STUDY; DS1 LIKE NSP2 GENE; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC REASSORTMENT; GENOTYPE; HUNGARY; LABORATORY TEST; MOLECULAR EPIDEMIOLOGY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PREVALENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAVIRUS; VIRUS DETECTION; VIRUS GENE; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS STRAIN; VIRUS TRANSMISSION; VP3 GENE; VP4 GENE; VP6 GENE; VP7 GENE; CLASSIFICATION; COMMUNICABLE DISEASE; DNA SEQUENCE; GENETICS; GEOGRAPHIC MAPPING; HEALTH SURVEY; HISTORY; HUMAN; MOLECULAR GENETICS; PHYLOGEOGRAPHY; ROTAVIRUS INFECTIONS; SPATIOTEMPORAL ANALYSIS; VIROLOGY;

ROTAVIRUS;

CAPSID PROTEINS; COMMUNICABLE DISEASES, EMERGING; GENOME, VIRAL; GENOTYPE; GEOGRAPHIC MAPPING; HISTORY, 21ST CENTURY; HUMANS; HUNGARY; MOLECULAR SEQUENCE DATA; PHYLOGENY; PHYLOGEOGRAPHY; POPULATION SURVEILLANCE; ROTAVIRUS; ROTAVIRUS INFECTIONS; SEQUENCE ANALYSIS, DNA; SPATIO-TEMPORAL ANALYSIS;

EID: 84912123705     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2014.09.016     Document Type: Article

References (44)

1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
2. Bányai K., Gentsch J.R., Glass R.I., Uj M., Mihály I., Szücs G. Eight-year survey of human rotavirus strains demonstrates circulation of unusual G and P types in Hungary. J. Clin. Microbiol. 2004, 42:393-397.
3. Bányai K., Gentsch J.R., Schipp R., Jakab F., Bene J., Melegh B., Glass R.I., Szucs G. Molecular epidemiology of human P[8], G9 rotaviruses in Hungary between 1998 and 2001. J. Med. Microbiol. 2004, 53:791-801.
4. Bányai K., Gentsch J.R., Schipp R., Jakab F., Meleg E., Mihály I., Szücs G. Dominating prevalence of P[8], G1 and P[8], G9 rotavirus strains among children admitted to hospital between 2000 and 2003 in Budapest, Hungary. J. Med. Virol. 2005, 76:414-423.
5. Bányai K., Bogdán A., Kisfali P., Molnár P., Mihály I., Melegh B., Martella V., Gentsch J.R., Szücs G. Emergence of serotype G12 rotaviruses, Hungary. Emerg. Infect. Dis. 2007, 13:916-919.
6. Bányai K., Bogdán A., Domonkos G., Kisfali P., Molnár P., Tóth A., Melegh B., Martella V., Gentsch J.R., Szucs G. Genetic diversity and zoonotic potential of human rotavirus strains, 2003-2006, Hungary. J. Med. Virol. 2009, 81:362-370.
7. Bányai K., Martella V., Molnár P., Mihály I., Van Ranst M., Matthijnssens J. Genetic heterogeneity in human G6P[14] rotavirus strains detected in Hungary suggests independent zoonotic origin. J. Infect. 2009, 59:213-215.
8. Bányai K., Esona M.D., Kerin T.K., Hull J.J., Mijatovic S., Vasconez N., Torres C., de Filippis A.M.B., Gentsch J.R. Molecular characterization of a rare, human-porcine reassortant rotavirus strain, G11P[6], from Ecuador. Arch. Virol. 2009, 154:1823-1829.
9. Bányai K., Esona M.D., Mijatovic S., Kerin T.K., Pedreira C., Mercado J., Balmaseda A., Perez M.C., Patel M.M., Gentsch J.R. Zoonotic bovine rotavirus strain in a diarrheic child, Nicaragua. J. Clin. Virol. 2009, 46:391-393.
10. Bányai K., Papp H., Dandár E., Molnár P., Mihály I., Van Ranst M., Martella V., Matthijnssens J. Whole genome sequencing and phylogenetic analysis of a zoonotic human G8P[14] rotavirus strain. Infect. Genet. Evol. 2010, 10:1140-1144.
11. Bányai K., László B., Vojdani J., Steele A.D., Gentsch J.R., Parashar U.D. 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, 30S:A122-130.
12. Bányai K., Borzák R., Ihász K., Fehér E., Dán A., Jakab F., Papp T., Hetzel U., Marschang R.E., Farkas S.L. Whole-genome sequencing of a green bush viper reovirus reveals a shared evolutionary history between reptilian and unusual mammalian orthoreoviruses. Arch. Virol. 2014, 159:153-158.
13. Buttery J.P., Lambert S.B., Grimwood K., Nissen M.D., Field E.J., Macartney K.K., Akikusa J.D., Kelly J.J., Kirkwood C.D. Reduction in rotavirus-associated acute gastroenteritis following introduction of rotavirus vaccine into Australia's National Childhood vaccine schedule. Pediatr. Infect. Dis. J. 2011, 30(1 Suppl.):S25-29.
14. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids. Res. 1988, 16:10881-10890.
15. Cowley D., Donato C.M., Roczo-Farkas S., Kirkwood C.D. Novel G10P[14] rotavirus strain, northern territory, Australia. Emerg. Infect. Dis. 2013, 19:1324-1327.
16. De Grazia S., Giammanco G.M., Potgieter C.A., Matthijnssens J., Banyai K., Platia M.A., Colomba C., Martella V. Unusual assortment of segments in 2 rare human rotavirus genomes. Emerg. Infect. Dis. 2010, 16:859-862.
17. Dennehy P.H. Rotavirus vaccines: an overview. Clin. Microbiol. Rev. 2008, 21:198-208.
18. DiStefano D.J., Kraiouchkine N., Mallette L., Maliga M., Kulnis G., Keller P.M., Clark H.F., Shaw A.R. Novel rotavirus VP7 typing assay using a one-step reverse transcriptase PCR protocol and product sequencing and utility of the assay for epidemiological studies and strain characterization, including serotype subgroup analysis. J. Clin. Microbiol. 2005, 43:5876-5880.
19. Djikeng A., Halpin R., Kuzmickas R., Depasse J., Feldblyum J., Sengamalay N., Afonso C., Zhang X., Anderson N.G., Ghedin E., Spiro D.J. Viral genome sequencing by random priming methods. BMC Genomics 2008, 9:5.
20. Dóró, R., László, B., Martella, V., Leshem, E., Gentsch, J., Parashar, U., Bányai, K., 2014. Review of global rotavirus strain prevalence data from six years post vaccine licensure surveillance: is there evidence of strain selection from vaccine pressure? Infect. Genet. Evol., in press.
21. Estes M.K., Kapikian A.Z. Rotaviruses. Fields Virology 2007, 1917-1974. Lippincott Williams & Wilkins, USA. fifth ed. D.M. Knipe, P.M. Howley (Eds.).
22. Gentsch J.R., Glass R.I., Woods P., Gouvea V., Gorziglia M., Flores J., Das B.K., Bhan M.K. Identification of group A rotavirus gene 4 types by polymerase chain reaction. J. Clin. Microbiol. 1992, 30:1365-1373.
23. Gentsch J.R., Laird A.R., Bielfelt B., Griffin D.D., Banyai K., Ramachandran M., Jain V., Cunliffe N.A., Nakagomi O., Kirkwood C.D., Fischer T.K., Parashar U.D., Bresee J.S., Jiang B., Glass R.I. Serotype diversity and reassortment between human and animal rotavirus strains: implications for rotavirus vaccine programs. J. Infect. Dis. 2005, 192(Suppl. 1):S146-159.
24. Giammanco G.M., Bonura F., Zeller M., Heylen E., Van Ranst M., Martella V., Bányai K., Matthijnssens J., De Grazia S. Evolution of DS-1-like human G2P[4] rotaviruses assessed by complete genome analyses. J. Gen. Virol. 2014, 95:91-109.
25. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids. Symp. Ser. 1999, 41:95-98.
26. László B., Kónya J., Dandár E., Deák J., Farkas Á., Gray J., Grósz G., Iturriza-Gomara M., Jakab F., Juhász Á., Kisfali P., Kovács J., Lengyel G., Martella V., Melegh B., Mészáros J., Molnár P., Nyúl Z., Papp H., Pátri L., Puskás E., Sántha I., Schneider F., Szomor K., Tóth A., Tóth E., Szucs G., Bányai K. Surveillance of human rotaviruses in 2007-2011, Hungary: exploring the genetic relatedness between vaccine and field strains. J. Clin. Virol. 2012, 55:140-146.
27. Maes P., Matthijnssens J., Rahman M., Van Ranst M. RotaC: a web-based tool for the complete genome classification of group A rotaviruses. BMC Microbiol. 2009, 9:238.
28. Matthijnssens J., Ciarlet M., Rahman M., Attoui H., Bányai K., Estes M.K., Gentsch J.R., Iturriza-Gómara M., Kirkwood C.D., Martella V., Mertens P.P., Nakagomi O., Patton J.T., Ruggeri F.M., Saif L.J., Santos N., Steyer A., Taniguchi K., Desselberger U., Van Ranst M. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol. 2008, 153:1621-1629.
29. Matthijnssens J., Bilcke J., Ciarlet M., Martella V., Bányai K., Rahman M., Zeller M., Beutels P., Van Damme P., Van Ranst M. Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol. 2009, 4:1303-1316.
30. Matthijnssens J., De Grazia S., Piessens J., Heylen E., Zeller M., Giammanco G.M., Bányai K., Buonavoglia C., Ciarlet M., Martella V., Van Ranst M. Multiple reassortment and interspecies transmission events contribute to the diversity of feline, canine and feline/canine-like human group A rotavirus strains. Infect. Genet. Evol. 2011, 11:1396-1406.
31. McDonald S.M., Davis K., McAllen J.K., Spiro D.J., Patton J.T. Intra-genotypic diversity of archival G4P[8] human rotaviruses from Washington, DC. Infect. Genet. Evol. 2011, 11:1586-1594.
32. 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. Diversity and relationships of cocirculating modern human rotaviruses revealed using large-scale comparative genomics. J. Virol. 2012, 86:9148-9162.
33. Mladenova Z., Papp H., Lengyel G., Kisfali P., Steyer A., Steyer A.F., Esona M.D., Iturriza-Gómara M., Bányai K. Detection of rare reassortant G5P[6] rotavirus, Bulgaria, Bulgaria. Infect. Genet. Evol. 2012, 12:1676-1684.
34. Nakagomi O., Kaga E., Gerna G., Sarasini A., Nakagomi T. Subgroup I serotype 3 human rotavirus strains with long RNA pattern as a result of naturally occurring reassortment between members of the bovine and AU-1 genogroups. Arch. Virol. 1992, 126:337-342.
35. Nakagomi O., Kaga E., Nakagomi T. Human rotavirus strain with unique VP4 neutralization epitopes as a result of natural reassortment between members of the AU-1 and Wa genogroups. Arch. Virol. 1992, 127:365-371.
36. Nicholas K.B., Nicholas H.B., Deerfield D.W. GeneDoc: analysis and visualization of genetic variation. EMBnet News 1997, 4:1-4.
37. Papp H., Borzák R., Farkas S., Kisfali P., Lengyel G., Molnár P., Melegh B., Matthijnssens J., Jakab F., Martella V., Bányai K. Zoonotic transmission of reassortant porcine G4P[6] rotaviruses in Hungarian pediatric patients identified sporadically over a 15 year period. Infect. Genet. Evol. 2013, 19:71-80.
38. Quaye O., McDonald S., Esona M.D., Lyde F.C., Mijatovic-Rustempasic S., Roy S., Banegas D.J., Quiñonez Y.M., Chinchilla B.L., Santiago F.G., Lozano H.G., Rey-Benito G., de Oliveira L.H., Gentsch J.R., Bowen M.D. Rotavirus G9P[4] in 3 countries in Latin America, 2009-2010. Emerg. Infect. Dis. 2013, 19:1332-1333.
39. Szücs G., Matson D.O., Uj M., Kukán E., Mihály I., Jelenik Z., Estes M.K. Group A rotavirus G type prevalence in two regions of Hungary. Arch. Virol. 1995, 140:1693-1703.
40. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
41. Wang F.T., Mast T.C., Glass R.J., Loughlin J., Seeger J.D. Effectiveness of the pentavalent rotavirus vaccine in preventing gastroenteritis in the United States. Pediatrics 2010, 125:e208-213.
42. Weinberg G.A., Teel E.N., Mijatovic-Rustempasic S., Payne D.C., Roy S., Foytich K., Parashar U.D., Gentsch J.R., Bowen M.D. Detection of novel rotavirus strain by vaccine postlicensure surveillance. Emerg. Infect. Dis. 2013, 19:1321-1323.
43. Wu F.T., Bányai K., Huang J.C., Wu H.S., Chang F.Y., Yang J.Y., Hsiung C.A., Huang Y.C., Lin J.S., Hwang K.P., Jiang B., Gentsch J.R. Diverse origin of P[19] rotaviruses in children with acute diarrhea in Taiwan: detection of novel lineages of the G3, G5, and G9 VP7 genes. J. Med. Virol. 2011, 83:1279-1287.
44. Wu F.T., Bányai K., Wu H.S., Yang D.C., Lin J.S., Hsiung C.A., Huang Y.C., Hwang K.P., Jiang B., Gentsch J.R. Identification of a G8P[14] rotavirus isolate obtained from a Taiwanese child: evidence for a relationship with bovine rotaviruses. Jpn. J. Infect. Dis. 2012, 65:455-457.