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Journal of Clinical Microbiology, March 2001, p. 1157-1160, Vol. 39, No. 3
Departamento de Virologia, Instituto de
Microbiologia, Universidade Federal do Rio de Janeiro, Rio de
Janeiro, RJ 21.941-590,1 and
Departamento de Microbiologia, Universidade Federal Fluminense,
Niterói, RJ 24.300-000,2 Brazil;
Center for Biologics Evaluation and Research, Food and Drug
Administration, Kensington, Maryland 208953; and
Laboratory of Infectious Diseases, National Institutes of
Health, Bethesda, Maryland 208924
Received 14 September 2000/Returned for modification 21 November
2000/Accepted 21 December 2000
Human rotavirus strains belonging to genotype G9 or P[9] were
detected in a collection of stool specimens from children with diarrhea
in two cities of the state of Rio de Janeiro, Brazil, between March
1997 and December 1999. G9 strains were first detected in April 1997 and remained prevalent until the end of the study, at a frequency of
15.9% (n = 157). A high percentage of VP7 nucleotide (99.0 to 99.5%) and deduced amino acid identity (98.6 to 99.1%) was
found between three randomly selected Brazilian G9 strains and the
American G9 strain US1205. A novel G9:P[4] genotype combination was
detected in addition to G9:P[8] and G9:P[6], demonstrating that this G genotype may undergo constant genetic reassortment in
nature. The P[9] rotavirus strains constituted 10.2%, the majority of which were detected between April and July 1997. The RNA
electrophoretic migration pattern of the G3:P[9] strains resembled
that of AU-1 virus (G3:P3[9]), suggesting a genetic similarity
between the Brazilian G3:P[9] strains and the Japanese virus, which
is similar to a feline rotavirus genetically.
Rotaviruses are the major etiologic
agents of infantile diarrhea worldwide (15). Epidemiologic
studies have demonstrated that rotavirus serotypes G1, G2, G3, and
G4 are the most-common types associated with disease globally, and
therefore they are the targets for vaccine development (13,
15). Recently, unusual rotavirus serotypes and genotypes have
been described in association with diarrhea in various parts of the
world. These include serotype G5 in Brazil (9, 17); G8 in
Malawi (5), Kenya (21), South Africa
(34), the United Kingdom (34), Nigeria
(1), and Australia (24); and G9 in India
(27), the United Sates (28), Bangladesh
(36), Malawi (5), the United Kingdom, (4), Australia (25), France (2),
and Ireland (22). The P specificity of a rotavirus
is usually more conservative than its G specificity; P1A[8] is the
most common serotype detected worldwide, followed by P1B[4] and
P2A[6] (13). A rotavirus strain belonging to serotype
P3[9] was first identified in Japan and was demonstrated to be
closely related to feline rotavirus strains genetically (20,
35). The P[9] rotavirus strains have been detected more often
in Japan (14, 37) than in other parts of the world such as
Venezuela (32), Italy (32), Malaysia (29), Brazil (17), Israel (31),
South Africa (33), Guinea-Bissau (7), and the
United States (12). The P[9] isolates are most commonly
associated with either G1 (K8-like) or G3 (AU-1-like) serotypes, except
for one isolate from Guinea-Bissau which bears a G4 specificity
(7).
One hundred fifty-seven (23%; n = 678)
rotavirus-positive stool samples from children under 5 years of age
with acute diarrhea (32 inpatients and 646 outpatients) were collected
between March 1997 and December 1999, at four centers in the city of
Rio de Janeiro, Brazil, and one center in the neighboring city of
Niterói in the state of Rio de Janeiro. The five centers are
located in areas of distinct levels of sanitation and
socioeconomic backgrounds. The presence of rotavirus in those samples
was determined by polyacrylamide electrophoresis analysis (PAGE)
and/or latex agglutination test. Rotavirus double-stranded RNA was
extracted from the stool samples and analyzed by reverse
transcription-PCR for determination of G and P specificity by using
primers specific for genotypes G1 to G6, G8 to G10, G12, P[4],
P[6], P[8], P[9], and P[10] (6, 8, 10, 11).
Twenty-five of 157 samples (15.9%) were typed as rotavirus genotype
G9: 19 were single infections, while 5 were mixed infections with the
G1 and G3 genotypes and 1 had a mixture of G9 and an untyped G genotype
(Table 1). The G9 samples were detected
in all five centers. Twenty samples were from outpatient children, and
five were from inpatient children. One single strain was detected in
April 1997, and the remaining 24 samples were detected between July
1998 and December 1999. Eight of the 25 G9 samples were detected in a
middle-class area, 8 were detected in a wealthy area, 8 were detected
in two centers that attend a poor population in the city of Rio de
Janeiro, and 1 sample was detected in a middle-class child from
Niterói. Nine G9 samples were detected in 1998, which constituted
25.0% of the total samples (n = 36) analyzed for that
year, and fifteen G9 samples were detected in 1999, which constituted
27.7% of the total samples (n = 54) analyzed for that
year, making it the second-most-prevalent G genotype in 1999 in Rio de
Janeiro (data not shown).
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.3.1157-1160.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Rotavirus Strains Bearing Genotype G9 or P[9] Recovered from
Brazilian Children with Diarrhea from 1997 to 1999
ABSTRACT
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TABLE 1.
Human rotavirus G9 genotype strains detected in the
cities of Rio de Janeiro and Niterói, Brazil, from 1997 to 1999
Three G9 samples (R143, R146, and R160) were randomly selected, and the
VP7-encoding gene of each virus was sequenced and compared to other G9
rotavirus VP7 gene sequences available in the GenBank. The best match
was with the American G9 strain US1205, which exhibited 99.0 to 99.5%
nucleotide and 98.6 to 99.1% deduced amino acid identity (Table
2). The phylogenetic analysis of the nucleotide sequences revealed the existence of at least three different VP7 gene clusters among rotavirus G9 strains. One
cluster was formed by the three Brazilian G9 strains, the
American strain US1205, and the strain Mc345 from Thailand; the second
cluster represented by the American strain WI61 and the Japanese strain F45; and the third cluster was formed by the Indian strain 116E (Fig.
1). Interestingly, the existence of minor
VP7 antigenic differences has recently been reported among selected G9
viruses belonging to each of the three VP7 gene clusters reported here (3, 16).
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A large diversity was observed with regard to the VP4 specificity of the Brazilian G9 strains. Although the majority of the G9 isolates carried P[8] specificity, strains bearing P[4] or P[6] specificity were also detected (Table 1). Thus far, rotavirus serotype G9 has been associated with VP4 genotype P[6], P[8], P[11], or P[19] (2, 6, 23, 25, 28). Here we found a G9 rotavirus isolate bearing the P[4] genotype. It is believed to be the first detection of such a G:P genotype combination. Rotavirus strains bearing G9 specificity have been previously described in Brazil on only three occasions: one isolate was detected in an infant (18), and the other isolates were detected in pigs (26, 30). The detection of rotavirus genotype G9 strains with such remarkable frequency among diarrheal patients (15.9%) in the last 2 years demonstrates that such a rotavirus genotype is an emerging pathogen in this country.
Sixteen of 157 (10.2%) samples were typed as rotavirus genotype
P[9]: seven single infections and nine mixed infections (Table 3), all from outpatients. Twelve strains
were detected in 1997, eleven of them being detected during the period
from April to July and one being detected in October. Five of 12 samples were from one center in Niterói, and seven were from a
center in a wealthy area in the city of Rio de Janeiro. Three samples
were detected between July and September of 1998 in one center in Rio de Janeiro located in a middle-class area; one sample was detected in
January 1999 in a center in Rio de Janeiro that attends the poor
population of a slum.
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The 16 P[9] samples were adapted to growth in primary African green
monkey kidney cells (BioWhittaker, Walkersville, Md.) and
double-stranded RNAs of such viruses were analyzed by PAGE. Interestingly, 10 of 16 viruses demonstrated a characteristic AU-1-like
electropherotype (i.e., widely spaced genes 5 and 6 and genes 10 and
11) or a mixture of an AU-1-like pattern plus an additional RNA pattern
(Fig. 2). This observation suggests a
genetic similarity between the Brazilian G3:P[9] strains and the
Japanese AU-1 virus (G3:P3[9]), which is similar to feline rotavirus
genetically (19). Since (i) 6 of 16 P[9] samples had an
AU-1-like PAGE pattern with G3:P[9] specificity and (ii) 4 of 16 P[9] samples had a mixture of an AU-1-like PAGE pattern plus an
additional PAGE pattern, it is possible that the remaining 6 P[9]
samples which did not show the AU-1-like pattern may be naturally
occurring reassortants between the AU-1-like virus and non-AU-1-like
virus.
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Rotavirus P3[9] strains have been detected most commonly among nonhospitalized children with diarrhea (7, 31). Silberstein and colleagues (31) speculate that genotype P[9] viruses (i) infect children as a consequence of zoonotic infection by circulating feline rotaviruses or by reassortants formed between feline and human group A rotaviruses such as K8 strain and thus (ii) are attenuated to some extent in the human host and cause sporadic and mild infections in children. Unfortunately, we have no access to the clinical data of patients who shed P[9] viruses in this study, which might shed light on the severity of diarrhea caused by such a P genotype. However, it is noteworthy that none of 16 patients who shed P[9] viruses in this study required hospitalization. Before this study, the detection of the rotavirus P[9] genotype was reported in Brazil only once, where three isolates were detected in a collection of fecal samples obtained between 1982 and 1994 in the state of São Paulo (17). The detection of 11 samples in a short period of time, 4 consecutive months within the same year, suggests the possibility of the occurrence of one or maybe two (since the samples came from two different cities) small outbreaks.
Of note is the finding that no G5 rotavirus strains were detected during the 3-year study period (1997 to 1999) in two cities of the state of Rio de Janeiro. This was particularly surprising since the incidence of this genotype appeared to be increasing in Brazil in the last decade (9). Is the disappearance of the genotype G5 virus in this study area somehow related to the emergence of the genotype G9 virus? It will be important to continue rotavirus strain surveillance in this and other regions of Brazil to determine whether a similar phenomenon occurs in the country. The results described here should reinforce the importance of rotavirus G9 as an epidemiologically important serotype and intensify the need of considering it as a vaccine candidate.
Nucleotide sequence accession numbers. The sequences of the R143, R146, and R160 isolates were deposited in GenBank under the accession numbers AF274969, AF274970, and AF274971.
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ACKNOWLEDGMENTS |
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We thank Maria Odete O. Carvalho and Giovani C. V. Costa for supplying the stool samples used in this work; Ronald Jones, Jerri Ross, and Mariam Wagner for their expert technical assistance; and Albert Kapikian for encouragement throughout the study.
This study was partially supported by CNPq, FINEP, FAPERJ, and FUJB, Brazil.
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FOOTNOTES |
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* Corresponding author. Mailing address: Departamento de Virologia, Instituto de Microbiologia, Universidade Federal do Rio de Janeiro, Cidade Universitária, CCS-Bl. I, Ilha do Fundão, Rio de Janeiro-RJ, 21.941-590, Brazil. Phone: 55 021 260-9311. Fax: 55 021 560-8344. E-mail: imvinos{at}microbio.ufrj.br.
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Journal of Clinical Microbiology, March 2001, p. 1157-1160, Vol. 39, No. 3
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.3.1157-1160.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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