SciELO - Scientific Electronic Library Online

 
vol.106 issue8Immunodetection of Helicobacter sp. and the associated expression of ABO blood group antigens in the gastric mucosa of captive and free-living New World primates in the Amazon regionBiological, biochemical and molecular features of Trypanosoma cruzi strains isolated from patients infected through oral transmission during a 2005 outbreak in the state of Santa Catarina, Brazil: its correspondence with the new T. cruzi Taxonomy Consensus (2009) author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

  • English (pdf)
  • Article in xml format
  • How to cite this article
  • SciELO Analytics
  • Curriculum ScienTI
  • Automatic translation

Indicators

Related links

Share


Memórias do Instituto Oswaldo Cruz

Print version ISSN 0074-0276

Mem. Inst. Oswaldo Cruz vol.106 no.8 Rio de Janeiro Dec. 2011

https://doi.org/10.1590/S0074-02762011000800008 

ARTICLES

 

Genetic diversity of noroviruses in Brazil

 

 

Julia Monassa Fioretti; Mônica Simões Rocha Ferreira; Matias Victoria; Carmen Baur Vieira; Maria da Penha Trindade Pinheiro Xavier; José Paulo Gagliardi Leite; Marize Pereira Miagostovich+

Laboratório de Virologia Comparada e Ambiental, Instituto Oswaldo Cruz-Fiocruz, Rio de Janeiro, RJ, Brasil

 

 


ABSTRACT

Norovirus (NoV) infections are a major cause of acute gastroenteritis outbreaks around the world. In Brazil, the surveillance system for acute diarrhoea does not include the diagnosis of NoV, precluding the ability to assess its impact on public health. The present study assessed the circulation of NoV genotypes in different Brazilian states by partial nucleotide sequencing analysis of the genomic region coding for the major capsid viral protein. NoV genogroup II genotype 4 (GII.4) was the prevalent (78%) followed by GII.6, GII.7, GII.12, GII.16 and GII.17, demonstrating the great diversity of NoV genotypes circulating in Brazil. Thus, this paper highlights the importance of a virological surveillance system to detect and characterize emerging strains of NoV and their spreading potential.

Key words: norovirus - genotypes - gastroenteritis - Brazil


 

 

Noroviruses (NoVs) are one of the major causes of acute gastroenteritis worldwide. In developing countries, these viruses are responsible for up to 1.1 million hospitalizations and have an estimated mortality rate of approximately 218,000 deaths per year (Patel et al. 2008). It is transmitted faeco-orally by ingesting contaminated food and water. However, infection can also occur through person-person contact, fomites or by aerosols produced during vomiting (Fankhauser et al. 2002, Koopmans et al. 2002, Lopman et al. 2002, Marks et al. 2003). These infections are often reported in nursing homes, kindergartens, hospitals, schools, cruise ships, restaurants, military installations and resorts (Leuenberger et al. 2007, Podewils et al. 2007, Rizzo et al. 2007, Verhoef et al. 2008).

NoVs are composed of a non-enveloped capsid with a single-stranded, positive-sense 7.7 kb RNA genome that encodes for three open reading frames (ORF). ORF-1 encodes a polyprotein that is cleaved post-translationally into non-structural proteins, including the RNA-dependent RNA polymerase (polymerase). The ORF-2 encodes viral protein (VP)1 that comprises the viral capsid and ORF-3 contains the VP2 gene, believed to be involved in genomic RNA packaging and virion assembly (Hardy 2005).

The Norovirus genus belongs to the Caliciviridae family and is divided into five genogroups (G); GI, GII and GIV have been shown to infect humans. Additionally, these genogroups can be further differentiated into more than 25 genotypes, based on the similarity between ORF-2 (Zheng et al. 2006).

NoV GII.4 is the most prevalent genotype and has been associated with global epidemics since the mid-1990s, mainly due to the emergence of new variants of GII.4 lineages that occurs in two-four-year intervals (Siebenga et al. 2007, 2009, Zheng et al. 2010).

Since the 1990s, the development of amplification protocols for different genomic regions, denominated regions A and B (ORF-1), C, D and E (ORF-2), has resulted in a NoV diagnostic breakthrough in several countries (Ando et al. 1995, Green et al. 1995, Noel et al. 1997, Fankhauser et al. 2002, Kojima et al. 2002, Vennema et al. 2002, Vinjé et al. 2004). A global electronic network surveillance of NoV, Noronet (noronet.nl), was established following an agreement between three networks involved in molecular surveillance of NoV: the Australian and New Zealand NoV Surveillance Network, the Foodborne Viruses in Europe Network and the CaliciNet in USA. This electronic surveillance system includes molecular and epidemiological data on NoV from different countries, as well as an automatic genotyping tool in which sequences of any region of the NoV genome can be entered and classified using phylogenetic methods. This approach enables the identification of the emergence of new epidemic strains around the world, demonstrating the importance of NoVs as agents of outbreaks and sporadic cases of acute gastroenteritis worldwide (Kroneman et al. 2011). In Brazil, the impact of NoVs is underestimated. Diagnostic and epidemiologic data are obtained mainly from research institutions, which demonstrates the importance of NoVs in communities and hospitalized children (Gabbay et al. 1994, Parks et al. 1999, Gallimore et al. 2004, Borges et al. 2006, Soares et al. 2007, Victoria et al. 2007, Ferreira et al. 2008, 2010, Xavier et al. 2009, Barreira et al. 2010, Luchs et al. 2011, Morillo et al. 2011). The aim of this study is to determine the NoV genotypes detected in different Brazilian states and to assess the genetic diversity of those viruses by raising NoV samples previously characterized. This study also highlights the importance of consolidating detection methods and molecular characterization to contribute to the establishment of a surveillance network that enhances the study of NoVs in Brazil and also worldwide.

 

SUBJECTS, MATERIALS AND METHODS

Study area - Brazil is a federation composed of 26 states and the Federal District (DF), Brasília. The states and the DF were grouped into regions that are merely geographical, with no political or administrative divisions, as follows: the North Region [states of Acre (AC), Amazonas, Amapá, Pará, Rondônia, Roraima and Tocantins], the Northeast Region [Alagoas (AL), Bahia (BA), Ceará (CE), Maranhão (MA), Paraíba, Pernambuco, Piauí, Rio Grande do Norte (RN) and Sergipe (SE)], the Central-West Region [Goiás, Mato Grosso, Mato Grosso do Sul (MS) and DF], the Southeast Region [Espírito Santo (ES), Minas Gerais (MG), Rio de Janeiro (RJ) and São Paulo (SP)] and the South Region [Paraná, Rio Grande do Sul (RS) and Santa Catarina].

Stool samples - A total of 90 stool samples positively diagnosed for NoV by reverse transcriptase-polymerase chain reaction (RT-PCR) of the B region (Fankhauser et al. 2002) was selected for this study in order to include samples that represent all regions of Brazil. Stool samples were obtained from acute gastroenteritis, sporadic or outbreak cases that occurred in different regions of the country between 2005-2009. Patients ranged in age from two months to 51 years old. All samples were processed at the Laboratory of Comparative and Environmental Virology and this study was approved by the Research Ethical Committee (311/2006) of Oswaldo Cruz Foundation.

RNA extraction - Viral RNA was extracted from 400 mL of a 10% (w/v) faecal suspension in Tris-Ca2+ buffer, pH 7.2, by the guanidine isothiocyanate/silica method, as described by Boom et al. (1990), with modifications introduced by Cardoso et al. (2002), and/or with a QIAmp® viral RNA Mini kit (QIAGEN®, Valencia, CA, USA) according to the manufacturer's instructions. The synthesis of complementary DNA was carried out using a random primer, pd(N)6 (Amersham Biosciences, UK).

Molecular characterization - RT-PCR was performed in all 90 positive samples for NoV using a set of primers that target a partial region (D) of the genome that encodes the main capsid protein, VP1, which is situated in ORF-2 (Vinjé et al. 2004). First, PCR was performed for GII using a primer set including Cap C, Cap D1 and Cap D3. For negative samples, a new PCR for GI using the primer set including Cap A, Cap B1 and Cap B2 was performed. The amplicons obtained were purified with a QIAquick® PCR Purification Kit (QIAGEN®, Valencia, CA, USA) following the manufacturer's recommendations and later quantified on a Nanodrop spectrophotometer (Thermo Scientific®, USA) or by 1% agarose gel electrophoresis using the Low DNA Mass Ladder (Invitrogen®, Carlsbad, CA, USA) as a molecular marker. The set of primers used to obtain the PCR amplicon were employed individually for gene sequencing. DNA sequencing was performed by the dideoxynucleotide chain termination method, using the ABI Prism Big Dye Terminator Cycle Sequencing Ready Reaction Kit 1, v. 3.1 and the ABI Prism 3730 Genetic Analyzer (both from Applied Biosystems®, Foster City, CA, USA) by the Genomic Platform of DNA sequencing PDTIS/Fiocruz.

Phylogenetic analysis - The nucleotide sequence data reported in this study were submitted to GenBank under accession: JN587115-JN587176. Sequence editing and multiple alignments were performed with the BioEdit Sequence Editor 7.0 software (Hall 1999). Phylogenetic trees were structured by the neighbour-joining method based on the Kimura two-parameter model (Kimura 1980) using the MEGA v.4.0 software package (Tamura et al. 2007). Confidence values of the internal nodes were calculated by bootstrap analyses using 1,000 replicates.

 

RESULTS

Sixty-four (71%) out of 90 samples studied were positive for GII and 26 were negative for both the GI and GII. Fig. 1 shows the genotyping of NoV strains analysed in this study. Of 64 samples sequenced and genotyped, 29 were included in the phylogenetic tree, representing all identified genotypes according to their origin and year of collection. Samples presenting 100% nucleotide identity were represented by only one sample. The genotypes found were GII.4 (n = 50), GII.6 (n = 5), GII.7 (n = 1), GII.12 (n = 4), GII.16 (n = 1) and GII.17 (n = 2). One strain could not be genotyped.

 

 

Table shows the quantity, origin and genotypes of sequenced samples. NoV GII.4 strains were observed in nine out of 13 states investigated. Strains GII.16 and GII.17 were detected to circulate in August and September 2005 in AC (North Region). Another strain found circulating in 2005 was GII.7, from the DF (Central-West Region). GII.12 was detected in 2009 in SE (Northeast Region), MG (Southeast Region) and RS (South Region).

The molecular characterization shows GII.4 strains grouping into three variants: 2004, 2006a and 2006b (Fig. 1). The 2006a and 2006b variants were represented by two large clusters: (i) the first composed with samples from MA, RN, AL, CE, BA, SE (Northeast Region) and MG (Southeast Region) during 2007-2009 (ii) and the second represented the 2006b variant grouped samples from AL, BA (Northeast Region), MS (Central-West Region) and MG (Southeast Region).

To assess the diversity of NoV circulating in the country, a survey of NoV nucleotide sequences available in GenBank was conducted. Fig. 2 illustrates a summary of all NoVs genotyped by region D from Brazil between 1995-1999 and 2004-2009, including results from this study and others previously published.

 

 

DISCUSSION

The characterization of NoVs into genogroups and genotypes was established by sequencing the complete genomic region coding for the VP1 capsid protein. To be classified into a genogroup or a genotype, the lineages must have a 55% and 85% similarity in amino acid sequence of the entire VP1 protein, respectively (Zheng et al. 2006). Since a correlation was established between the complete nucleotide sequence of VP1 and a partial nt sequence (region D) (Vinjé et al. 2004), this region has been used to genotype NoV. The comparison of different strains has been hampered by the use of different approaches for molecular characterization of NoV (Victoria et al. 2007, Ferreira et al. 2008, 2010, Bruggink & Marshall 2009, Nataraju et al. 2010).

Global NoV analysis was performed by grouping the nucleotide sequences obtained in this study with all previous NoV VP1 region D sequences from Brazilian strains for which data was available on GenBank (Castilho et al. 2006, Victoria et al. 2007, Ferreira et al. 2008, 2010, Barreira et al. 2010). The data analysis showed a great diversity of NoV strains circulating in the country, including GI.2, GI.3, GI.6, GII.2, GII.3, GII.4, GII.6, GII.7, GII.8, GII.12, GII.14, GII.16 and GII.17.

NoV GII.4 was the most prevalent genotype detected and was identified in 50 out of 64 sequenced strains and in nine out of 13 states evaluated. These results are in agreement with prior studies published in other countries (Iritani et al. 2010, Pang et al. 2010) and Brazil (Barreira et al. 2010, Ferreira et al. 2010). Three GII.4 variants were found circulating in Brazil, showing its breadth of diversity and distribution. The high prevalence of GII.4 worldwide has been explained to be a result of point mutations that originated as new variants and replaced previous variants (Siebenga et al. 2009). This is probably due to the absence of protective immunity in the susceptible community, causing new outbreaks of acute gastroenteritis; this allows the GII.4 genotype to remain a prevalent strain. The GII.4 variant substitution phenomenon was observed in all continents throughout the investigation period (Siebenga et al. 2009, Motomura et al. 2010, Zheng et al. 2010).

This analysis was the first to identify the genotypes GII.12, GII.16 and GII.17 in Brazil. The GII.16 and GII.17 strains were found circulating simultaneously during a Rotavirus-A G9 gastroenteritis outbreak that occurred in 2005 in AC (North Region) (Siqueira et al. 2010, Tort et al. 2010). These genotypes were also found circulating in South Korea, 2007/2008 (GII.16), Argentina, 2005/2006, and Thailand, 2006/2007 (GII.17) (Gomes et al. 2008, Chung et al. 2010, Kittigul et al. 2010). In Brazil, GII.12 was observed circulating in three different regions: Northeast, Southeast and South. However, there are a few reports of NoV GII.12 worldwide, including Japan in 2001/2002 and 2004/2005 (Fukuda et al. 2010). Further, in the United States this genotype was responsible for 16% of all reported NoV outbreaks during the winter of 2009/2010 (Vega & Vinjé 2011) and, in Vietnam, GII.12 was found in hospitalized children at a higher prevalence than GII.4 (Tamura et al. 2010).

Regarding other NoV genotypes, GII.7 was detected in 2005 in the DF and RJ (Ferreira et al. 2010). GII.6 circulated in PE (Northeast Region), ES, MG, RJ and SP (Southeast Region) from 2003-2004 and 2007-2008 (Castilho et al. 2006, Barreira et al. 2010, Ferreira et al. 2010).

GI.2, 3 and 6 and GII.2, 3, 8 and 14 NoV characterized by region D were previously described in other Brazilian studies; however, these genotypes were not found in the present study. GI has been described as a genogroup that circulates to a lesser extent than GII (Castilho et al. 2006, Victoria et al. 2007, Barreira et al. 2010, Ferreira et al. 2010). The evaluation of outbreaks that occurred in Japan during 2002-2006 revealed that only one out of 12 outbreaks was caused by GI (Shinkawa et al. 2008).

In Brazil, other NoV molecular characterization studies have been carried out. However, they could not be included in the phylogenetic analysis because nucleotide sequencing and genotyping was performed in regions that encode for RNA dependent-RNA polymerase, known as region A and B of the genome (Parks et al. 1999, Gallimore et al. 2004, Borges et al. 2006, Campos et al. 2008, Luchs et al. 2011, Morillo et al. 2011).

The impact of NoV infections in outbreaks and sporadic cases of acute gastroenteritis has been characterized by the emergence of novel strains, which have been identified using new protocols that allow for the rapid diagnosis and molecular characterization of those viruses. Protocols using primers that amplify regions A and B have been widely used for viral detection because this is a highly conserved region (Ando et al. 1995, Jiang et al. 1999, Fankhauser et al. 2002). Still, regions C and D, which comprise different partial sequences of the gene encoding for VP1 protein, are recommended for the characterization of different genotypes (Mattison et al. 2009). Region D, used in this study, was previously described to efficiently genotype NoV for characterization and has been used as an alternative to full sequencing of VP1 that relies on about 1,600 nucleotides (Vinjé et al. 2004). The high genetic variability of region D may explain why we failed to amplify all previously detected strains by the polymerase conserved region. Recently, Mattison et al. (2009) suggested the use of region C for genotype characterization and region D for characterizing variants of GII.4 samples. Certainly, new protocols for NoV characterization will emerge in order to increase the number of genotyped samples that encompass more variants of NoV. Further studies using different set of primers or complete VP1 sequencing must be performed in order to achieve this goal.

In conclusion, new studies should be conducted to standardize and validate protocols for NoV diagnosis that allow for the establishment of NoV networks, which will demonstrate the true impact of these infections in developing countries, as well as facilitate future molecular epidemiology and viral evolution studies.

 

ACKNOWLEDGEMENTS

To Rosane Maria Santos de Assis, Alexandre Madi Fialho and Juliana Andrade, for technical assistance, and to the staff of Central State Laboratories, Municipal Gastroenteritis Surveillance Program and the General Coordination of Laboratories/Ministry of Health, for providing samples for this study.

 

REFERENCES

Ando T, Monroe S, Gentsch JR, Jin Q, Lewis DC, Glass RI 1995. Detection and differentiation of antigenically distinct small roundstructured viruses (Norwalk-like viruses) by reverse transcription-PCR and southern hybridization. J Clin Microbiol 33: 64-71.         [ Links ]

Barreira DM, Ferreira MS, Fumian TM, Checon R, de Sadovsky AD, Leite JP, Miagostovich MP, Spano LC 2010. Viral load and genotypes of noroviruses in symptomatic and asymptomatic children in southeastern Brazil. J Clin Virol 47: 60-64.         [ Links ]

Boom R, Sol CJ, Salimans MM, Jansen CL, Wertheim-van Dillen PM, van der Noordaa J 1990. Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28: 495-503.         [ Links ]

Borges AM, Teixeira JM, Costa PS, Giugliano LG, Fiaccadori FS, Franco RC, Brito WM, Leite JP, Cardoso DD 2006. Detection of calicivirus from fecal samples from children with acute gastroenteritis in the West Central Region of Brazil. Mem Inst Oswaldo Cruz 101: 721-724.         [ Links ]

Bruggink LD, Marshall JA 2009. Molecular and epidemiological features of GIIb norovirus outbreaks in Victoria, Australia, 2002-2005. J Med Virol 81: 1652-1660.         [ Links ]

Campos GS, Moreau VH, Bandeira A, Barberino G, Almeida PF, Amador DM, de Lima MO, Sardi S 2008. Molecular detection and genetic diversity of norovirus in hospitalized young adults with acute gastroenteritis in Bahia, Brazil. Arch Virol 153: 1125-1129.         [ Links ]

Cardoso D, Fiaccadori FS, Souza M, Martins RM, Leite JP 2002. Detection and genotyping of astroviruses from children with acutegastroenteritis from Goiânia, Goiás, Brazil. Med Sci Monit 8: 624-628.         [ Links ]

Castilho JG, Munford V, Resque HR, Fagundes-Neto U, Vinjé J, Rácz ML 2006. Genetic diversity of norovirus among children with gastroenteritis in São Paulo state, Brazil. J Clin Microbiol 44: 3947-3953.         [ Links ]

Chung JY, Han TH, Park SH, Kim SW, Hwang ES 2010. Detection of GII-4/2006b variant and recombinant noroviruses in children with acute gastroenteritis, South Korea. J Med Virol 82: 146-152.         [ Links ]

Fankhauser RL, Monroe SS, Noel JS, Humphrey CD, Bresee JS, Parashar UD, Ando T, Glass RI 2002. Epidemiological and molecular trends of "Norwalk-like viruses" associated with outbreaks of gastroenteritis in the United States. J Infect Dis 186: 1-7.         [ Links ]

Ferreira MS, Victoria M, Carvalho-Costa FA, Vieira CB, Xavier MP, Fioretti JM, Andrade J, Volotão EM, Rocha M, Leite JP, Miagostovich MP 2010. Surveillance of norovirus infections in the state of Rio de Janeiro, Brazil 2005-2008. J Med Virol 82: 1442-1448.         [ Links ]

Ferreira MS, Xavier MP, Fumian TM, Victoria M, Oliveira SA, Pena LH, Leite JP, Miagostovich MP 2008. Acute gastroenteritis cases associated with noroviruses infection in the state of Rio de Janeiro. J Med Virol 80: 338-344.         [ Links ]

Fukuda S, Takao S, Shigemoto N, Tanizawa Y, Seno M 2010. Transition of genotypes associated with norovirus gastroenteritis outbreaks in a limited area of Japan, Hiroshima Prefecture, during eight epidemic seasons. Arch Virol 155: 111-115.         [ Links ]

Gabbay YB, Glass RI, Monroe SS, Carcamo C, Estes MK, Mascarenhas JD, Linhares AC 1994. Prevalence of antibodies to Norwalk virus among Amerindians in isolated Amazonian communities. Am J Epidemiol 139: 728-733.         [ Links ]

Gallimore CI, Barreiros MA, Brown DW, Nascimento JP, Leite JP 2004. Noroviruses associated with acute gastroenteritis in a children's day care facility in Rio de Janeiro, Brazil. Braz J Med Biol Res 37: 321-326.         [ Links ]

Gomes KA, Stupka JA, Diana A, Parra GI 2008. Molecular characterization of calicivirus strains detected in outbreaks of gastroenteritis occurring in Argentina during 2005 and 2006. Rev Argent Microbiol 40: 222-228.         [ Links ]

Green SM, Lambden PR, Deng Y, Lowes JA, Lineham S, Bushell J, Rogers J, Caul EO, Ashley CR, Clarke IN 1995. Polymerase chain reaction detection of small round-structure viruses from two related hospital outbreaks of gastroenteritis usin inosine-containing primers. J Med Virol 45: 197-202.         [ Links ]

Hall TA 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.         [ Links ]

Hardy ME 2005. Norovirus protein structure and function. FEMS Microbiol Lett 253: 1-8.         [ Links ]

Iritani N, Kaida A, Kubo H, Abe N, Goto K, Ogura H, Seto Y 2010. Molecular epidemiology of noroviruses detected in seasonal outbreaks of acute nonbacterial gastroenteritis in Osaka City, Japan, from 1996-1997 to 2008-2009. J Med Virol 82: 2097-2105.         [ Links ]

Jiang X, Huang PW, Zhong WM, Farkas T, Cubitt DW, Matson DO 1999. Design and evaluation of a primer pair that detects both Norwalk and Sapporo-like caliciviruses by RT-PCR. J Virol Methods 83: 145-154.         [ Links ]

Kimura MA 1980. Simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111-120.         [ Links ]

Kittigul L, Pombubpa K, Taweekate Y, Diraphat P, Sujirarat D, Khamrin P, Ushijima H 2010. Norovirus GII-4 2006b variant circulating in patients with acute gastroenteritis in Thailand during a 2006-2007 study. J Med Virol 82: 854-860.         [ Links ]

Kojima S, Kageyama T, Fukushi S, Hoshino FB, Shinohara M, Uchida K, Natori K, Takeda N, Katayama K 2002. Genogroup-speciûc PCR primers for detection of Norwalk-like viruses. J Virol Methods 100: 107-114.         [ Links ]

Koopmans M, von Bonsdorff CH, Vinjé J, de Medici D, Monroe S 2002. Foodborne viruses. FEMS Microbiol Rev 26: 187-205.         [ Links ]

Kroneman A, Vennema H, Deforche K, Avoort HV, Peñaranda S, Oberste MS, Vinjé J, Koopmans M 2011. An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol 51: 121-125.         [ Links ]

Leuenberger S, Widdowson MA, Feilchenfeldt J, Egger R, Streuli RA 2007. Norovirus outbreak in a district general hospital - new strain identified. Swiss Med Wkly 137: 57-81.         [ Links ]

Lopman BA, Brown DW, Koopmans M 2002. Human calicivirus in Europe. J Clin Virol 24: 137-160.         [ Links ]

Luchs A, Morillo SG, Ribeiro CD, Vilanova BC, Calux SJ, Carmona RC, Timenetsky MST 2011. Gastroenteritis outbreak due to G2P[4] rotavirus and GII norovirus at two correctional facilities in Brazil, 2010. J Clin Virol 51: 213-214.         [ Links ]

Marks PJ, Vipond IB, Regan FM, Wedgwood K, Fey RE, Caul EO 2003. A school outbreak of Norwalk-like virus: evidence for airborne transmission. Epidemiol Infect 131: 727-736.         [ Links ]

Mattison K, Grudeski E, Auk B, Charest H, Drews SJ, Fritzinger A, Gregoricus N, Hayward S, Houde A, Lee BE, Pang XL, Wong J, Booth TF, Vinjé J 2009. Multicenter comparison of two norovirus ORF2-based genotyping protocols. J Clin Microbiol 47: 3927-3932.         [ Links ]

Morillo SG, Luchs A, Cilli A, Ribeiro CD, Calux SJ, Carmona R de C, Timenetsky Mdo C 2011. Large gastroenteritis outbreak due to norovirus GII in São Paulo, Brazil, summer 2010. Rev Inst Med Trop Sao Paulo 53: 119-120.         [ Links ]

Motomura K, Yokoyama M, Ode H, Nakamura H, Mori H, Kanda T, Oka T, Katayama K, Noda M, Tanaka T, Takeda N, Sato H 2010. Divergent evolution of norovirus GII/4 by genome recombination from May 2006 to February 2009 in Japan. J Virol 84: 8085-8097.         [ Links ]

Nataraju SM, Pativada M, Chatterjee D, Nayak MK, Ganesh B, Bhattacharya MK, Ramamurthy T, Ganguly S, Saha DR, Rajendran K, Ghosh M, Kobayashi N, Krishnan T 2010. Molecular epidemiology of norovirus infections in children and adults: sequence analysis of region C indicates genetic diversity of NVGII strains in Kolkata, India. Epidemiol Infect 19: 1-9.         [ Links ]

Noel JS, Ando T, Leite JP, Green KY, Dingle KE, Estes MK, Seto Y, Monroe SS, Glass RI 1997. Correlation of patient immune responses with genetically characterized small round-structured viruses involved in outbreaks of nonbacterial acute gastroenteritis in the United States, 1990 to 1995. J Med Virol 53: 372-383.         [ Links ]

Pang XL, Preiksaitis JK, Wong S, Li V, Lee BE 2010. Influence of novel norovirus GII.4 variants on gastroenteritis outbreak dynamics in Alberta and the northern territories, Canada between 2000 and 2008. PLoS ONE 5: e11599.         [ Links ]

Parks CG, Moe CL, Rhodes D, Lima A, Barrett L, Tseng F, Baric R, Talal A, Guerrant R 1999. Genomic diversity of "Norwalk like viruses" (NLVs): pediatric infections in a Brazilian shantytown. J Med Virol 58: 426-434.         [ Links ]

Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinjé J, Parashar UD 2008. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14: 1224-1231.         [ Links ]

Podewils LJ, Zanardi Blevins L, Hagenbuch M, Itani D, Burns A, Otto C, Blanton L, Adams S, Monroe SS, Beach MJ, Widdowson M 2007. Outbreak of norovirus illness associated with a swimming pool. Epidemiol Infect 135: 827-833.         [ Links ]

Rizzo C, Di Bartolo I, Santantonio M, Coscia MF, Monno R, De Vito D, Ruggeri FM, Rizzo G 2007. Epidemiological and virological investigation of a Norovirus outbreak in a resort in Puglia, Italy. BMC Infect Dis 7: 135.         [ Links ]

Shinkawa N, Noda M, Yoshizumi S, Tokutake Y, Shiraishi T, Arita-Nishida T, Nishio O, Oka T, Hansman GS, Takeda N, Kimura H 2008. Molecular epidemiology of noroviruses detected in food handler-associated outbreaks of gastroenteritis in Japan. Intervirology 51: 422-426.         [ Links ]

Siebenga JJ, Vennema H, Renckens B, de Bruin E, van der Veer B, Siezen RJ, Koopmans M 2007. Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J Virol 81: 9932-9941.         [ Links ]

Siebenga JJ, Vennema H, Zheng DP, Vinjé J, Lee BE, Pang XL, Ho EC, Lim W, Choudekar A, Broor S, Halperin T, Rasool NB,Hewitt J, Greening GE, Jin M, Duan ZJ, Lucero Y, O'Ryan M, Hoehne M, Schreier E, Ratcliff RM, White PA, Iritani N, Reuter G, Koopmans M 2009. Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001-2007. J Infect Dis 200: 802-812.         [ Links ]

Siqueira AA, Santelli AC, Alencar LR Jr, Dantas MP, Dimech CP, Carmo GM, Santos DA, Alves RM, Lucena MB, Morais M, Assis RM, Fialho A, Mascarenhas JD, Costa M, Linhares AC, Leite JP, Araujo WN, Hatch DL 2010. Outbreak of acute gastroenteritis in young children with death due to rotavirus genotype G9 in Rio Branco, Brazilian Amazon Region, 2005. Int J Infect Dis 14: e898-903.         [ Links ]

Soares CC, Santos N, Beard RS, Albuquerque MC, Maranhão AG, Rocha LN, Ramírez ML, Monroe SS, Glass RI, Gentsch J 2007. Norovirus detection and genotyping for children with gastroenteritis, Brazil. Emerg Infect Dis 13: 1244-1246.         [ Links ]

Tamura K, Dudley J, Nei M, Kumar S 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.         [ Links ]

Tamura T, Nishikawa M, Anh DD, Suzuki H 2010. Molecular epidemiological study of rotavirus and norovirus infections among children with acute gastroenteritis in Nha Trang, Vietnam, December 2005-June 2006. Jpn J Infect Dis 63: 405-411.         [ Links ]

Tort LF, Volotão Ede M, de Mendonça MC, da Silva MF, Siqueira AA, Assis RM, Moratorio G, Cristina J, Leite JP 2010. Phylogenetic analysis of human P[8]G9 rotavirus strains circulating in Brazil reveals the presence of a novel genetic variant. J Clin Virol 47: 345-355.         [ Links ]

Vega E, Vinjé J 2011. Novel GII.12 Norovirus Strain, United States, 2009-2010. Emerg Infect Dis 17: 1516-1518.         [ Links ]

Vennema H, de Bruin E, Koopmans M 2002. Rational optimization of generic primers used for Norwalk-like virus detection by reverse transcriptase polymerase chain reaction. J Clin Virol 25: 233-235.         [ Links ]

Verhoef L, Depoortere E, Boxman I, Duizer E, van Duynhoven Y, Harris J, Johnsen C, Kroneman A, Le Guyader S, Lim W,Maunula L, Meldal H, Ratcliff R, Reuter G, Schreier E, Siebenga J, Vainio K, Varela C, Vennema H, Koopmans M, Food Borne Viruses in Europe Network 2008. Food borne viruses in Europe network. Emergence of new norovirus variants on spring cruise ships and prediction of winter epidemics. Emerg Infect Dis 14: 238-243.         [ Links ]

Victoria M, Carvalho-Costa FA, Heinemann MB, Leite JP, Miagostovich M 2007. Prevalence and molecular epidemiology of noroviruses in hospitalized children with acute gastroenteritis in Rio de Janeiro, Brazil, 2004. Pediatr Infect Dis J 26: 1-5.         [ Links ]

Vinjé J, Hamidjaja RA, Sobsey MD 2004. Development and application of a capsid VP1 (region D) based on reverse transcription PCR assay for genotyping of a genogroup I and II noroviruses. J Virol Methods 116: 109-117.         [ Links ]

Xavier MP, Oliveira SA, Ferreira MS, Victoria M, Miranda V, Silva MF, Strina A, Barreto ML, Miagostovicht MP, Leite JP 2009. Detection of caliciviruses associated with acute infantile gastroenteritis in Salvador, an urban center in Northeast Brazil. Braz J Med Biol Res 42: 438-444.         [ Links ]

Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS 2006. Norovirus classification and proposed strain nomenclature. Virology 346: 312-323.         [ Links ]

Zheng DP, Widdowson MA, Glass RI, Vinjé J 2010. Molecular epidemiology of genogroup II-genotype 4 noroviruses in the United States between 1994 and 2006. J Clin Microbiol 48: 168-177.         [ Links ]

 

 

Received 5 April 2011
Accepted 16 August 2011
Financial support: IOC-FIOCRUZ, CGLAB-SVS, CNPq, FAPERJ

 

 

MV present address: Laboratorio de Virología Molecular, Universidad de La República, Regional Norte, Salto, Uruguay
+ Corresponding author: marizepm@ioc.fiocruz.br

Creative Commons License All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License