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.
AltschulS. F.,
MaddenT. L.,
SchäfferA. A.,
ZhangJ.,
ZhangZ.,
MillerW.,
LipmanD. J.1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402[CrossRef]
AraújoI. T.,
FerreiraM. S. R.,
FialhoA. M.,
AssisR. M.,
CruzC. M.,
RochaM.,
LeiteJ. 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]
BányaiK.,
GentschJ. R.,
GlassR. I.,
ÚjM.,
MihályI.,
SzücsG.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]
BernsteinD. I.,
SmithV. E.,
SherwoodJ. R.,
SchiffG. M.,
SanderD. S.,
DeFeudisD.,
SpriggsD. R.,
WardR. L.1998; Safety and immunogenicity of live, attenuated human rotavirus vaccine 89-12. Vaccine 16:381–387[CrossRef]
BreseeJ. S.,
GlassR. I.,
IvanoffB.,
GentschJ. R.1999; Current status and future priorities for rotavirus vaccine development, evaluation and implementation in developing countries. Vaccine 17:2207–2222[CrossRef]
ClarkH. F.,
OffitP. A.,
EllisR. 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]
Clements-MannM. L.,
DudasR.,
HoshinoY. & 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]
CoulsonB.,
UnicombL. E.,
PitsonG. A.,
BishopR. F.1987; Simple and specific enzyme immunoassay using monoclonal antibodies for serotyping human rotaviruses. J Clin Microbiol 25:509–515
CunliffeN. A.,
DoveW.,
BunnJ. E. G.,
RamadamM. B.,
NyangaoJ. W. O.,
RiveronR. L.,
CuevasL. E.,
HartC. A.2001a; Expanding global distribution of rotavirus serotype G9: detection in Libya, Kenya, and Cuba. Emerg Infect Dis 7:890–892[CrossRef]
CunliffeN. A.,
GondweJ. S.,
GrahamS. M.,
ThindwaB. D. M.,
DoveW.,
BroadheadR. L.,
MolyneuxM. E.,
HartC. A.2001b; Rotavirus strain diversity in Blantyre. Malawi: from 1997 to 1999J Clin Microbiol 39:836–843[CrossRef]
DasB. K.,
GentschJ. R.,
HoshinoY.,
IshidaS.,
NakagomiO.,
BhanM. K.,
KumarR.,
GlassR. I.1993; Characterization of the G serotype and genogroup of New Delhi newborn rotavirus strain 116E. Virology 197:99–107[CrossRef]
DasB. K.,
GentschJ. R.,
CicirelloH. G.,
WoodsP. A.,
GuptaA.,
RamachandranM.,
KumarR.,
BhanM. K.,
GlassR. I.1994; Characterization of rotavirus strains from newborns in New Delhi, India. J Clin Microbiol 32:1820–1822
DolanK. T.,
TwistE. M.,
Horton-SlightP.,
ForrerC.,
BellL. M.Jr,
PlotkinS. A.,
ClarkH. F.1985; Epidemiology of rotavirus electropherotypes determined by a simplified diagnostic technique with RNA analysis. J Clin Microbiol 21:753–758
GentschJ. R.,
GlassR. I.,
WoodsP.,
GouveaV.,
GorzigliaM.,
FloresJ.,
DasB. K.,
BhanM. K.1992; Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 30:1365–1373
GentschJ. R.,
DasB. K.,
JlangB.,
BhanM. K.,
GlassR. I.1993; Similarity of the VP4 protein of human rotavirus strain 116E to that of the bovine B223 strain. Virology 194:424–430[CrossRef]
GentschJ. R.,
WoodsP. A.,
RamachandranM.,
DasB. K.,
LeiteJ. P.,
AlfieriA.,
KumarR.,
BhanM. K.,
GlassR. 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]
GlassR. I.,
BreseeJ. S.,
ParasharU. D.,
HolmanR. C.,
GentschJ. R.1999; First rotavirus vaccine licensed: is there really a need?. Acta Paediatr Suppl 88:2–8[CrossRef]
GouveaV.,
LimaR. C. C.,
LinharesR. E.,
ClarkH. F.,
NosawaC. M.,
SantosN.1999; Identification of two lineages (WA-like and F45-like) within the major rotavirus genotype P[8]. Virus Res 59:141–147[CrossRef]
GreenK. Y.,
HoshinoY.,
IkegamiN.1989; Sequence analysis of the gene encoding the serotype-specific glycoprotein (VP7) of two new human rotavirus serotypes. Virology 168:429–433[CrossRef]
GriffinD. D.,
KirkwoodC. D.,
ParasharU. D.,
WoodsP. A.,
BreseeJ. S.,
GlassR. I.,
GentschJ. 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
HoshinoY.,
KapikianA. Z.2000; Rotavirus serotypes: classification and importance in epidemiology, immunity, and vaccine development. J Health Popul Nutr 18:5–14
Iturriza-GómaraM.,
GreenJ.,
BrownD. W. G.,
RamsayM.,
DesselbergerU.,
GrayJ. J.2000; Molecular epidemiology of human group A rotavirus infections in the United Kingdom between 1995 and 1998. J Clin Microbiol 38:4394–4401
Iturriza-GómaraM.,
IsherwoodB.,
DesselbergerU.,
GrayJ.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]
Iturriza-GòmaraM.,
AndertonE.,
KangG.,
GallimoreC.,
PhillipsW.,
DesselbergerU.,
GrayJ.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]
JagannathM. R.,
VethanayagamR. R.,
ReddyB. S. Y.,
RamanS.,
RaoC. 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]
JainV.,
DasB. K.,
BhanM. K.,
GlassR. I.,
GentschJ. 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]
LairdA. R.,
GentschJ. R.,
NakagomiT.,
NakagomiO.,
GlassR. 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]
LarraldeG.,
FloresJ.1990; Identification of gene 4 alleles among human rotaviruses by polymerase chain reaction-derived probes. Virology 179:469–473[CrossRef]
MartellaV.,
TerioV.,
Del GaudioG.,
GentileM.,
FiorenteP.,
BarbutiS.,
BuonavogliaC.2003; Detection of the emerging rotavirus G9 serotype at high frequency in Italy. J Clin Microbiol 41:3960–3963[CrossRef]
MaunulaL.,
von BonsdorffC.-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
MaunulaL.,
von BonsdorffC.-H.2002; Frequent reassortments may explain the genetic heterogeneity of rotaviruses: analysis of Finnish rotavirus strains. J Virol 76:11793–11800[CrossRef]
NakagomiT.,
AkataniK.,
IkegamiN.,
KatsushimaN.,
NakagomiO.1988; Occurrence of changes in human rotavirus serotypes with concurrent changes in genomic RNA electropherotypes. J Clin Microbiol 26:2586–2592
NakagomiT.,
OhshimaA.,
AkataniK.,
IkegamiN.,
KatsushimaN.,
NakagomiO.1990; Isolation and molecular characterization of a serotype 9 human rotavirus strain. Microbiol Immunol 34:77–82[CrossRef]
NakagomiO.,
IsegawaY.,
WardR. L.,
KnowltonD. R.,
KagaE.,
NakagomiT.,
UedaS.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]
NguyenV. M.,
NguyenV. T.,
HuynhP. 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]
O'HalloranF.,
LynchM.,
CryanB.,
FanningS.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]
OkaT.,
NakagomiT.,
NakagomiO.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]
OkadaJ.,
UrasawaT.,
KobayashiN.,
TaniguchiK.,
HasegawaA.,
MiseK.,
UrasawaS.2000; New P serotype of group A human rotavirus closely related to that of a porcine rotavirus. J Med Virol 60:63–69[CrossRef]
RamachandranM.,
KirkwoodC. D.,
UnicombL.,
CunliffeN. A.,
WardR. L.,
BhanM. K.,
ClarkH. F.,
GlassR. I.,
GentschJ. R.2000; Molecular characterization of serotype G9 rotavirus strains from a global collection. Virology 278:436–444[CrossRef]
SantosN.,
LimaR. C. C.,
NozawaC. M.,
LinharesR. E.,
GouveaV.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
TaniguchiK.,
UrasawaT.,
MoritaY.,
GreenbergH. B.,
UrasawaS.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]
UnicombL. E.,
PodderG.,
GentschJ. R.,
WoodsP. A.,
HasanK. Z.,
FaruqueA. S. G.,
AlbertM. J.,
GlassR. 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
UrasawaS.,
HasegawaA.,
UrasawaT. & 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]
WiddowsonM.-A.,
van DoornumG. J. J.,
van der PoelW. H. M.,
de BoerA. S.,
MahdiU.,
KoopmansM.2000; Emerging group-A rotavirus and a nosocomial outbreak of diarrhoea. Lancet 356:1161–1162[CrossRef]
WyattR. G.,
JamesH. D.Jr,
PittmanA. L.,
HoshinoY.,
GreenbergH. B.,
KalicaA. R.,
FloresJ.,
KapikianA. Z.1983; Direct isolation in cell culture of human rotaviruses and their characterization into four serotypes. J Clin Microbiol 18:310–317
ZhouY.,
SupawadeeJ.,
KhamwanC. & 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]
ZhouY.,
LiL.,
OkitsuS.,
ManeekarnN.,
UshijimaH.2003; Distribution of human rotaviruses, especially G9 strains, in Japan from 1996 to 2000. Microbiol Immunol 47:591–599[CrossRef]
ZizdicS.,
RidjanovicZ.,
MasicI.1992; Newly discovered rotavirus serotypes in 4 years of collecting samples from children with diarrheal syndromes. Medicinski Arhiv 45:15–18