Group A rotavirus and norovirus display sharply distinct
               seasonal profiles in Belém, northern Brazil

Siqueira, Jones Anderson Monteiro; Linhares, Alexandre da Costa; Gonçalves, Maryelle dos Santos; Carvalho, Thaís Cristina Nascimento de; Justino, Maria Cleonice Aguiar; Mascarenhas, Joana D'Arc Pereira; Gabbay, Yvone Benchimol

doi:10.1590/S0074-02762013000500020

Abstract

Several viruses have been associated with acute gastroenteritis (AGE), and group A rotavirus (RVA) and nor-ovirus (NoV) are the most prevalent. This study aimed to assess their prevalence among children hospitalised for diarrhoea during a three-year surveillance study. From May 2008-April 2011, overall positivity rates of 21.6% (628/2904) and 35.4% (171/483) were observed for RVA and NoV, respectively. The seasonality observed indicated distinct patterns when both viruses were compared. This finding may explain why hospitalisation for AGE remains constant throughout the year. Continuous AGE monitoring is needed to better assess the patterns of infection.

rotavirus; norovirus; seasonality

Several viruses have been associated with acute gastroenteritis (AGE) in humans and the most prevalent are group A rotavirus (RVA) and norovirus (NoV). RVA and NoV often cause disease that may require hospitalisation and this translates into a significant public health burden (Clark & McKendrick 2004).

According to the International Committee on Taxonomy of Viruses, rotaviruses are members of the Reoviridae family and are subdivided into five serological species (A-E) and two tentative species (F-G) based on the antigenic properties of the VP6 protein (Attoui et al. 2012) and VP6 sequence-based cut-off values. Groups A, B and C are associated with infection in humans and a variety of animals (Matthijnssens et al. 2012).

RVA is the most common cause of AGE and requires medical attention or hospitalisation for young children worldwide, accounting for approximately 2.4 million hospitalisations, and more than half a million deaths annually among children less than five years of age (Tate et al. 2012).

RVA tends to be more common in cooler, drier months in most settings, but seasonal peaks have been noted year round in different areas and can differ over time in the same location (Levy et al. 2009). Attempts to relate these patterns to climatic variables, such as temperature, humidity and rainfall, have led to conflicting results (D'Souza et al. 2008). Many developing countries are located in the tropics, where traditionally RVA activity has been thought to lack seasonality, leading to high levels of year-round disease transmission (Cook et al. 1990). However, a recent study conducted in Belém, state of Pará, northern Brazil, Amazon Region, on children hospitalised in the same clinic studied in this study reinforced a possible seasonality for this virus (Justino et al. 2011).

NoV belongs to the Caliciviridae family, which also includes four other genera: Sapovirus, Vesivirus, Lagovirus and Nebovirus. While Norovirus and Sapovirus are known to infect humans, the remainder are mainly of veterinary interest (Clark et al. 2012).

Studies estimate that every year NoV is responsible for 900,000 episodes of AGE, requiring clinic visits and 64,000 hospitalisations of children less than five years of age in economically developed countries. In developing countries, more than 1.1 million hospitalisations and 128,000 deaths per year are believed to be associated with NoV (Patel et al. 2008).

Seasonal variation in NoV infection is a recognised, albeit poorly understood, phenomenon (Rohayem 2009). NoV epidemic characteristics and timing are markedly consistent from year to year, with a peak incidence during the wintertime (from October-April) and specific peaks in February and March. However, outbreaks of NoV do occur during summer (Verhoef et al. 2008). The temporal distribution is most likely based on biological, environmental and behavioural factors that regulate the transmission, virulence and persistence of the virions in host populations (Rohayem 2009).

In view of the importance of RVA and NoV as causes of AGE that may require hospitalisation, this cross-sectional study aimed to assess the prevalence of RVA and NoV among children hospitalised for AGE during a three-year surveillance study.

The surveillance of community-acquired AGE was conducted in a large paediatric hospital located in Belém from May 2008-April 2011. Approximately 40% of all paediatric hospitalisations for AGE in Belém occur in this hospital.

Eligible cases for inclusion were children aged less than five years who were hospitalised for AGE and presented diarrhoea, which was defined as the presence of ≥ 3 liquid or semi-liquid stools in a 24-h period. Only faecal samples collected up to 48 h following admission were tested for the presence of RVA and NoV.

A total of 2,904 samples were obtained during the study period and screened for RVA antigen using a commercial Ridascreen^(r) Rotavirus enzyme-immunoassay (EIA) (R-Biopharm, Darmstadt, Germany). Reverse transcription polymerase chain reaction (RT-PCR) was used to determine the RVA G and P types (Gentsch et al. 1992).

Of 2276 RVA-negative samples with sufficient material, a representative number of 483 samples (≅ 20%) was randomly selected on a monthly basis for NoV testing. NoV was detected using a third-generation commercial Ridascreen^(r) Norovirus EIA (R-Biopharm, Darmstadt, Germany) and RT-PCR using a pool of primers (Mon 432/434-431/433) specific for the polymerase region, which detected GI and GII, respectively (Anderson et al. 2001). The samples were tested with EIA and RT-PCR using the same faecal suspension and those with positive results with at least one method were considered positive. Subsequently, only amplicons of positive samples that displayed clear bands were selected for genotyping by nucleotide sequencing using the same primers used for PCR.

Statistical analysis was performed using BioEstat 5.0 software (Ayres et al. 2007). The variation between the RVA and NoV prevalence rates was analysed using the Mann-Whitney U test in the months in which higher differences in positivity were observed. p-values < 0.05 were regarded as statistically significant. The study was approved by the Ethical Research Committee in Humans of the Evandro Chagas Institute (0003.0.072.000-08 and 0024.0.072.000-10).

From May 2008-April 2011, an overall positivity of 21.6% (628/2904) was found for RVA using EIA. NoV was detected in 35.4% (171/483) of samples using both EIA and RT-PCR.

RVA infections were more prevalent in August 2008 (48%) and April 2009 (46.6%). For NoV, three prevalence peaks were observed throughout the study period: September and October 2008 (63.6% each month) and February 2010 (62.1%). Figure shows the monthly RVA and NoV positivity rates during the three-year surveillance period.

Monthly distribution of group A rotavirus (RVA) and norovirus (NoV) detected in faecal specimens from children hospitalised with acute gastroenteritis from May 2008-April 2011 in Belém, state of Pará, northern Brazil, Amazon Region. #: number of samples tested by month; *: statistically significant differences between RAV and NoV prevalence [December 2008 (p = 0.0034), February 2010 (p < 0.0001) and 2011 (p = 0.0311) ]; **: horizontal dashed lines represent the triennial means of percentages for both viruses.

Statistical analyses were performed for the months in which higher prevalence differences between RVA and NoV were found. Significant differences were observed in December 2008 and February 2010 and 2011.

With regard to G2P[4] during the first year (May 2008-May 2009), the findings essentially reflected those of a previous vaccine effectiveness study, in which this serotype accounted for 82% (441/538) of isolates (Justino et al. 2011). During this same period, the RNA polymerase region was sequenced in 22 (31.9%) of the 69 NoV-positive samples, of which 90.9% (20/22) were genotype GII.4d and 9.1% (2/22) were genotype GII.b (Siqueira et al. 2013).

RVA tends to be more common in cooler, drier months in most settings, but seasonal peaks have been noted in different countries and can vary over time in the same country (Levy et al. 2009). Many studies have described an increase in the rates of NoV infection in the winter months in temperate countries. In contrast, in tropical countries, NoV infection is observed year round and does not show a clear seasonal pattern (Fretz et al. 2005).

The seasonality observed for both pathogens suggests sharply distinct seasonal profiles and a "seesaw effect" was observed between the two viruses. This finding may explain why hospitalisations for AGE occur throughout the year. Similar results were observed in 2003 by González et al. (2011) in Venezuela, a region geographically close to northern Brazil, where marked and opposite seasonal patterns were observed.

Although an effective RVA vaccine is available, no vaccine exists for NoV, making it difficult to control the infection. When sample collection began in this study (2008), the RVA vaccination coverage was 89.9% for the first dose and 76.4% for the second dose (Leite et al. 2008). These rates did not increase significantly during the following years of the study.

NoV occurred at apparently higher rates than RVA. However, it should be noted that only RVA-negative samples were tested for NoV and this may not reflect the true NoV incidence rate, but rather the proportion of NoV-positive cases among RVA-negative patients. A weakness of this study was that possible mixed RVA and NoV infection was not identified, leading to possible overestimation. However, it is noteworthy that this sampling criterion is often used in Brazil and some other countries (Soares et al. 2007 Andreasi et al. 2008, Le et al. 2010, Mahar & Kirkwood 2011).

The RVA G2P[4] detected in this study also showed natural re-emergence in Latin America and many other parts of the world (Antunes et al. 2009, Munford et al. 2009). A review conducted by Patel et al. (2008) in different localities, including Latin America, over 18 years (1990-2008) concluded that NoV GII.4 was responsible for 75-100% of cases of AGE, including both outbreaks and sporadic cases.

Previous publications have suggested a limited sensitivity of the NoV Ridascreen EIA kit, except for the GII.4 type (Okitsu-Negishi et al. 2006, Kirby et al. 2010). However, all samples tested by EIA were also tested by RT-PCR, which is a more sensitive method for detecting any NoV genotype. For this reason, the results may not have been significantly influenced by a possibly lower EIA sensitivity.

This study underscores the importance of NoV as a cause of endemic disease that may require hospitalisation. In fact, the continuous monitoring of RVA and NoV-related AGE is needed to better assess the pattern of these viral infections in Belém; in addition, a group of RVA-positive samples should be tested for the presence of NoV to detect mixed infections.

To the technical support provided by all the clinical operations team of the Effectiveness Project and by the work group of Viral Gastroenteritis Laboratory of the IEC, especially to Ana Beatriz Pedroza and Maria Silvia Lucena, to all Hospital Serzedelo Correa employees (formerly Clínica Pediátrica do Pará) who were involved in this study, to all the participating children and their parents/guardians, and to the Postgraduate Program in Tropical Diseases, Tropical Medicine Centre, Federal University of Pará State, whose author Jones Siqueira was affiliated during this study.

REFERENCES

Anderson AD, Garrett VD, Sobel J, Monroe SS, Fankhauser RL, Schwab KJ, Bresee JS, Mead PS, Higgins C, Campana J, Glass RI 2001. Multistate outbreak of Norwalk-like virus gastroenteritis associated with a common caterer. Am J Epidemiol 154: 1013-1019.
Andreasi MSA, Cardoso DDP, Fernandes SM, Tozetti IA, Borges AMT, Fiaccadori FS, Santos RAT, Souza M 2008. Adenovirus, calicivirus and astrovirus detection in fecal samples of hospitalized children with acute gastroenteritis from Campo Grande, MS, Brazil. Mem Inst Oswaldo Cruz 103: 741-744.
Antunes H, Afonso A, Iturriza M, Martinho I, Ribeiro C, Rocha S, Magalhães C, Carvalho L, Branca F, Gray J 2009. G2P[4] the most prevalent rotavirus genotype in 2007 winter season in an European non-vaccinated population. J Clin Virol 45: 76-78.
Attoui H, Mertens PPC, Becnel J, Belaganahalli S, Bergoin M, Brussaard CP, Chappell JD, Ciarlet M, Del Vas M, Dermody TS, Dormitzer PR, Duncan R, Fang Q, Grahan R, Guglielmi KM, Harding RM, Hillman B, Makkay A, Marzachì C, Matthijnssens J, Milne RG, Mohd Jaafar F, Mori H, Noordeloos AA, Omura T, Patton JT, Rao S, Maan M, Stoltz D, Suzuki N, Upadhyaya NM, Wei C, Zhou H 2012. Genus rotavirus. In AMQ King, MJ Adams, EB Carstens, Lefkowitz, virus taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses, Elsevier Academic Press, London, p. 603-613.
Ayres M, Ayres Jr M, Ayres DL, dos Santos ASS 2007. BioEstat 5.0: aplicações estatísticas nas áreas das ciências biológicas e médicas, 5th ed., Instituto de Desenvolvimento Sustentável Mamirauá - IDSM/MCT/CNPq, Belém, 364 pp.
Clark B, McKendrick M 2004. A review of viral gastroenteritis. Curr Opin Infect Dis 17: 461-469.
Clark IN, Estes MK, Green KY, Hansman GS, Knowles NJ, Koopmans MK, Matson DO, Meyers G, Neill JD, Radford A, Smith AW, Studdert MJ, Thiel HJ, Vinjé J 2012. Family Caliciviridae. In AMQ King, MJ Adams, EB Carstens, Lefkowitz, Virus taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses, Elsevier Academic Press, London, p. 977-986.
Cook SM, Glass RI, LeBaron CW, Ho MS 1990. Global seasonality of rotavirus infections. Health Organ Bull 68: 171-177.
D'Souza RM, Hall G, Becker NG 2008. Climatic factors associated with hospitalizations for rotavirus diarrhoea in children under 5 years of age. Epidemiol Infect 136: 56-64.
Fretz R, Herrmann L, Christen A, Svoboda P, Dubuis O, Viollier EH, Tanner M 2005. Frequency of norovirus in stool samples from patients with gastrointestinal symptoms in Switzerland. Eur J Clin Microbiol Infect Dis 24: 214-216.
Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M, Flores J, Das BK, Bhan MK 1992. Identification of groupA rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 30: 1365-1373.
González GG, Liprandi F, Ludert JE 2011. Molecular epidemiology of enteric viruses in children with sporadic gastroenteritis in Valencia, Venezuela. J Med Virol 83: 1972-1982.
Justino MCA, Linhares AC, Lanzieri TM, Miranda Y, Mascarenhas JD, Abreu E, Guerra SF, Oliveira AS, da Silva VB, Sanchez N, Meyer N, Shafi F, Ortega-Barria E, Soriano-Gabarró M, Colindres RE 2011. Effectiveness of the monovalent G1P8 human rotavirus vaccine against hospitalization for severe G2P4 rotavirus gastroenteritis in Belém, Brazil. Pediatr Infect Dis 30: 396-401.
Kirby A, Gurgel RQ, Dove W, Vieira SCF, Cunliffe NA, Cuevas LE 2010. An evaluation of the RIDASCREEN and IDEIA enzyme immunoassays and the RIDAQUICK immunochromatographic test for the detection of norovirus in faecal specimens. J Clin Virol 49: 254-257.
Le VP, Jung YC, Kang KS, Lim I, Myung SC, Kim W 2010. Genetic characterization of GII.4 2006b variants from Jeju Island, South Korea. J Med Virol 82: 1065-1070.
Leite JPG, Carvalho-Costa FA, Linhares AC 2008. Group A rotavirus genotypes and the ongoing Brazilian experience - A Review. Mem Inst Oswaldo Cruz 103: 745-753.
Levy K, Hubbard AE, Eisenberg JN 2009. Seasonality of rotavirus disease in the tropics: a systematic review and meta-analysis. Int J Epidemiol 38: 1487-1496.
Mahar JE, Kirkwood CD 2011. Characterization of norovirus strains in Australian Children from 2006 to 2008: prevalence of recombinant strains. J Med Virol 83: 2213-2219.
Matthijnssens J, Otto PH, Ciarlet M, Desselberger U, Ranst MV, Johne R 2012. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol 157: 1177-1182.
Munford V, Gilio AE, de Souza EC, Cardoso DM, Cardoso DD, Bor-ges AM, Costa PS, Melgaço IA, Rosa H, Carvalho PR, Goldani MZ, Moreira Jr ED, Santana C, El Khoury A, Ikedo F, Rácz ML 2009. Rotavirus gastroenteritis in children in 4 regions in Brazil: a hospital-based surveillance study. J Infect Dis 200 (Suppl.): S106-S113.
Okitsu-Negishi S, Okame M, Shimizu Y, Phan TG, Tomaru T, Kamijo S, Sato T, Yagyu F, Müller WEG, Ushijima H 2006. Detection of norovirus antigens from recombinant virus-like particles and stool samples by a commercial norovirus enzyme-linked immunosorbent assay kit. J Clin Microbiol 44: 3784-3786.
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 8: 1224-1231.
Rohayem J 2009. Norovirus seasonality and the potential impact of climate change. Clin Microbiol Infect 15: 524-527.
Siqueira JAM, Linhares AC, Carvalho TCN, Aragão GC, Oliveira DS, dos Santos MC, de Sousa MS, Justino MCA, Mascarenhas JDP, Gabbay YB 2013. Norovirus infection in children admitted to hospital for acute gastroenteritis in Belém, Pará, northern Brazil. J Med Virol 85: 737-744.
Soares CC, Santos N, Beard RS, Albuquerque MCM, 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.
Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD 2012. 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 12: 136-141.
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 2008. Emergence of new norovirus variants on spring cruise ships and prediction of winter epidemics. Emerg Infect Dis 14: 238-243.

Publication Dates

Publication in this collection
Aug 2013

History

Received
04 Oct 2012
Accepted
14 Feb 2013

[1] Anderson AD, Garrett VD, Sobel J, Monroe SS, Fankhauser RL, Schwab KJ, Bresee JS, Mead PS, Higgins C, Campana J, Glass RI 2001. Multistate outbreak of Norwalk-like virus gastroenteritis associated with a common caterer. Am J Epidemiol 154: 1013-1019.

[2] Andreasi MSA, Cardoso DDP, Fernandes SM, Tozetti IA, Borges AMT, Fiaccadori FS, Santos RAT, Souza M 2008. Adenovirus, calicivirus and astrovirus detection in fecal samples of hospitalized children with acute gastroenteritis from Campo Grande, MS, Brazil. Mem Inst Oswaldo Cruz 103: 741-744.

[3] Antunes H, Afonso A, Iturriza M, Martinho I, Ribeiro C, Rocha S, Magalhães C, Carvalho L, Branca F, Gray J 2009. G2P[4] the most prevalent rotavirus genotype in 2007 winter season in an European non-vaccinated population. J Clin Virol 45: 76-78.

[4] Attoui H, Mertens PPC, Becnel J, Belaganahalli S, Bergoin M, Brussaard CP, Chappell JD, Ciarlet M, Del Vas M, Dermody TS, Dormitzer PR, Duncan R, Fang Q, Grahan R, Guglielmi KM, Harding RM, Hillman B, Makkay A, Marzachì C, Matthijnssens J, Milne RG, Mohd Jaafar F, Mori H, Noordeloos AA, Omura T, Patton JT, Rao S, Maan M, Stoltz D, Suzuki N, Upadhyaya NM, Wei C, Zhou H 2012. Genus rotavirus. In AMQ King, MJ Adams, EB Carstens, Lefkowitz, virus taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses, Elsevier Academic Press, London, p. 603-613.

[5] Ayres M, Ayres Jr M, Ayres DL, dos Santos ASS 2007. BioEstat 5.0: aplicações estatísticas nas áreas das ciências biológicas e médicas, 5th ed., Instituto de Desenvolvimento Sustentável Mamirauá - IDSM/MCT/CNPq, Belém, 364 pp.

[6] Clark B, McKendrick M 2004. A review of viral gastroenteritis. Curr Opin Infect Dis 17: 461-469.

[7] Clark IN, Estes MK, Green KY, Hansman GS, Knowles NJ, Koopmans MK, Matson DO, Meyers G, Neill JD, Radford A, Smith AW, Studdert MJ, Thiel HJ, Vinjé J 2012. Family Caliciviridae. In AMQ King, MJ Adams, EB Carstens, Lefkowitz, Virus taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses, Elsevier Academic Press, London, p. 977-986.

[8] Cook SM, Glass RI, LeBaron CW, Ho MS 1990. Global seasonality of rotavirus infections. Health Organ Bull 68: 171-177.

[9] D'Souza RM, Hall G, Becker NG 2008. Climatic factors associated with hospitalizations for rotavirus diarrhoea in children under 5 years of age. Epidemiol Infect 136: 56-64.

[10] Fretz R, Herrmann L, Christen A, Svoboda P, Dubuis O, Viollier EH, Tanner M 2005. Frequency of norovirus in stool samples from patients with gastrointestinal symptoms in Switzerland. Eur J Clin Microbiol Infect Dis 24: 214-216.

[11] Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M, Flores J, Das BK, Bhan MK 1992. Identification of groupA rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 30: 1365-1373.

[12] González GG, Liprandi F, Ludert JE 2011. Molecular epidemiology of enteric viruses in children with sporadic gastroenteritis in Valencia, Venezuela. J Med Virol 83: 1972-1982.

[13] Justino MCA, Linhares AC, Lanzieri TM, Miranda Y, Mascarenhas JD, Abreu E, Guerra SF, Oliveira AS, da Silva VB, Sanchez N, Meyer N, Shafi F, Ortega-Barria E, Soriano-Gabarró M, Colindres RE 2011. Effectiveness of the monovalent G1P8 human rotavirus vaccine against hospitalization for severe G2P4 rotavirus gastroenteritis in Belém, Brazil. Pediatr Infect Dis 30: 396-401.

[14] Kirby A, Gurgel RQ, Dove W, Vieira SCF, Cunliffe NA, Cuevas LE 2010. An evaluation of the RIDASCREEN and IDEIA enzyme immunoassays and the RIDAQUICK immunochromatographic test for the detection of norovirus in faecal specimens. J Clin Virol 49: 254-257.

[15] Le VP, Jung YC, Kang KS, Lim I, Myung SC, Kim W 2010. Genetic characterization of GII.4 2006b variants from Jeju Island, South Korea. J Med Virol 82: 1065-1070.

[16] Leite JPG, Carvalho-Costa FA, Linhares AC 2008. Group A rotavirus genotypes and the ongoing Brazilian experience - A Review. Mem Inst Oswaldo Cruz 103: 745-753.

[17] Levy K, Hubbard AE, Eisenberg JN 2009. Seasonality of rotavirus disease in the tropics: a systematic review and meta-analysis. Int J Epidemiol 38: 1487-1496.

[18] Mahar JE, Kirkwood CD 2011. Characterization of norovirus strains in Australian Children from 2006 to 2008: prevalence of recombinant strains. J Med Virol 83: 2213-2219.

[19] Matthijnssens J, Otto PH, Ciarlet M, Desselberger U, Ranst MV, Johne R 2012. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol 157: 1177-1182.

[20] Munford V, Gilio AE, de Souza EC, Cardoso DM, Cardoso DD, Bor-ges AM, Costa PS, Melgaço IA, Rosa H, Carvalho PR, Goldani MZ, Moreira Jr ED, Santana C, El Khoury A, Ikedo F, Rácz ML 2009. Rotavirus gastroenteritis in children in 4 regions in Brazil: a hospital-based surveillance study. J Infect Dis 200 (Suppl.): S106-S113.

[21] Okitsu-Negishi S, Okame M, Shimizu Y, Phan TG, Tomaru T, Kamijo S, Sato T, Yagyu F, Müller WEG, Ushijima H 2006. Detection of norovirus antigens from recombinant virus-like particles and stool samples by a commercial norovirus enzyme-linked immunosorbent assay kit. J Clin Microbiol 44: 3784-3786.

[22] 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 8: 1224-1231.

[23] Rohayem J 2009. Norovirus seasonality and the potential impact of climate change. Clin Microbiol Infect 15: 524-527.

[24] Siqueira JAM, Linhares AC, Carvalho TCN, Aragão GC, Oliveira DS, dos Santos MC, de Sousa MS, Justino MCA, Mascarenhas JDP, Gabbay YB 2013. Norovirus infection in children admitted to hospital for acute gastroenteritis in Belém, Pará, northern Brazil. J Med Virol 85: 737-744.

[25] Soares CC, Santos N, Beard RS, Albuquerque MCM, 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.

[26] Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD 2012. 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 12: 136-141.

[27] 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 2008. Emergence of new norovirus variants on spring cruise ships and prediction of winter epidemics. Emerg Infect Dis 14: 238-243.

Group A rotavirus and norovirus display sharply distinct seasonal profiles in Belém, northern Brazil

Abstract

REFERENCES

Publication Dates

History