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Norovirus GII and astrovirus in shellfish from a mangrove region in Cananéia, Brazil: molecular detection and characterization

  • Food Microbiology - Research Paper
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Abstract

In recent years, annual cases of gastroenteritis have been reported in the world at high rates, suggesting an association with the consumption of shellfish with enteric viruses in their tissues. Anthropic activities are considered a source of environmental pollution and the main responsible for contamination by pathogenic microorganisms in aquatic environments. The objective of this study was to evaluate, by RT-semi-nested PCR, the presence of astrovirus (AstV) and norovirus genogroup II (NoV GII) in mussels (Mytella falcata) and oysters (Crassostrea brasiliana) collected in two sites of the Lagunar Complex of Cananéia, State of São Paulo, Brazil. A total of 150 samples of mussels and oysters (75 samples each) were analyzed. AstV was not identified in any shellfish sample. NoV GII was detected in 21 samples (14%), 8 mussel samples (38%), and 13 oyster samples (62%). From the 21 positive samples, 16 were analyzed by nucleotide sequencing. The molecular characterization revealed that Brazilian samples were grouped into clades along with other sequences from Brazil, Japan, and Mexico. There was 93.8–100% amino acid sequence similarity among the samples in this study and > 94.9% when compared with the strains isolated from clinical cases in Brazil. The screening of shellfish for the presence of health-significant enteric viruses can help prevent outbreaks among consumers and contribute to the improvement of the estuarine environment.

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References

  1. Di Renzo L, Colica C, Carraro A, Cenci Goga B, Marsella LT, Botta R et al (2015) Food safety and nutritional quality for the prevention of non communicable diseases: the Nutrient, hazard Analysis and Critical Control Point process (NACCP). J Transl Med 13:1–13. https://doi.org/10.1186/s12967-015-0484-2

    Article  Google Scholar 

  2. Leal Diego AG, Dores Ramos AP, Marques Souza DS, Durigan M, Greinert-Goulart JA, Moresco V et al (2013) Sanitary quality of edible bivalve mollusks in Southeastern Brazil using an UV based depuration system. Ocean Coast Manag 72:93–100. https://doi.org/10.1016/j.ocecoaman.2011.07.010

    Article  Google Scholar 

  3. da Rocha MP, Dourado PLR, Cardoso CAL, Cândido LS, Pereira JG, de Oliveira KMP et al (2018) Tools for monitoring aquatic environments to identify anthropic effects. Environ Monit Assess 190:1–13

    Article  Google Scholar 

  4. Ballesteros ML, Rivetti NG, Morillo DO, Bertrand L, Amé MV, Bistoni MA (2017) Multi-biomarker responses in fish (Jenynsia multidentata) to assess the impact of pollution in rivers with mixtures of environmental contaminants. Sci Total Environ 595:711–722

    Article  CAS  Google Scholar 

  5. Souza DSM, Dominot AFÁ, Moresco V, Barardi CRM (2018) Presence of enteric viruses, bioaccumulation and stability in Anomalocardia brasiliana clams (Gmelin, 1791). Int J Food Microbiol 266:363–371. https://doi.org/10.1016/j.ijfoodmicro.2017.08.004

    Article  PubMed  Google Scholar 

  6. El Nemr A, El-Said GF, Ragab S, Khaled A, El-Sikaily A (2016) The distribution, contamination and risk assessment of heavy metals in sediment and shellfish from the Red Sea coast. Egypt Chemosphere 165:369–380. https://doi.org/10.1016/j.chemosphere.2016.09.048

    Article  CAS  PubMed  Google Scholar 

  7. Marques JA, Silva de Assis HC, Guiloski IC, Sandrini-Neto L, Carreira RS, Lana PC, Antioxidant defense responses in Mytella guyanensis (Lamarck, (1819) exposed to an experimental diesel oil spill in Paranaguá Bay (Paraná, Brazil). Ecotoxicol Environ Saf 2014(107):269–275. https://doi.org/10.1016/j.ecoenv.2014.06.001

    Article  CAS  Google Scholar 

  8. Carter MJ (2005) Enterically infecting viruses: pathogenicity, transmission and significance for food and waterborne infection. J Appl Microbiol 98:1354–1380. https://doi.org/10.1111/j.1365-2672.2005.02635.x

    Article  CAS  PubMed  Google Scholar 

  9. Walker DI, Younger A, Stockley L, Baker-Austin C (2018) Escherichia coli testing and enumeration in live bivalve shellfish – present methods and future directions. Food Microbiol 73:29–38. https://doi.org/10.1016/j.fm.2017.12.006

    Article  PubMed  Google Scholar 

  10. Cormier J, Gutierrez M, Goodridge L, Janes M (2014) Concentration of enteric virus indicator from seawater using granular activated carbon. J Virol Methods 196:212–218

    Article  CAS  Google Scholar 

  11. FAO. FAO 2008.

  12. Torok V, Hodgson K, McLeod C, Tan J, Malhi N, Turnbull A (2018) National survey of foodborne viruses in Australian oysters at production. Food Microbiol 69:196–203. https://doi.org/10.1016/j.fm.2017.08.014

    Article  CAS  PubMed  Google Scholar 

  13. Campos CJA, Kershaw S, Morgan OC, Lees DN (2017) Risk factors for norovirus contamination of shellfish water catchments in England and Wales. Int J Food Microbiol 241:318–324. https://doi.org/10.1016/j.ijfoodmicro.2016.10.028

    Article  PubMed  Google Scholar 

  14. Mesquita JR, Vaz L, Cerqueira S, Castilho F, Santos R, Monteiro S et al (2011) Norovirus, hepatitis A virus and enterovirus presence in shellfish from high quality harvesting areas in Portugal. Food Microbiol 28:936–941. https://doi.org/10.1016/j.fm.2011.01.005

    Article  PubMed  Google Scholar 

  15. Bellou M, Kokkinos P, Vantarakis A (2013) Shellfish-borne viral outbreaks: a systematic review. Food Environ Virol 5:13–23. https://doi.org/10.1007/s12560-012-9097-6

    Article  CAS  PubMed  Google Scholar 

  16. Hodgson KR, Torok VA, Turnbull AR (2017) Bacteriophages as enteric viral indicators in bivalve mollusc management. Food Microbiol 65:284–293. https://doi.org/10.1016/j.fm.2017.03.003

    Article  CAS  PubMed  Google Scholar 

  17. Padovan AC, Neave MJ, Munksgaard NC, Gibb KS. Multiple approaches to assess the safety of artisanal marine food in a tropical estuary. Environ Monit Assess 2017;189. https://doi.org/10.1007/s10661-017-5842-5.

  18. La Rosa G, Fratini M, Vennarucci VS, Guercio A, Purpari G, Muscillo M (2012) GIV noroviruses and other enteric viruses in bivalves: a preliminary study. New Microbiol 35:27–34

    PubMed  Google Scholar 

  19. Le Guyader F, Neill FH, Estes MK, Monroe SS, Ando T, Atmar RL (1996) Detection and analysis of a small round-structured virus strain in oysters implicated in an outbreak of acute gastroenteritis. Appl Environ Microbiol 62:4268–4272. https://doi.org/10.1128/aem.62.11.4268-4272.1996

    Article  PubMed  PubMed Central  Google Scholar 

  20. Le Guyader FS, Neill FH, Dubois E, Bon F, Loisy F, Kohli E et al (2003) A semiquantitative approach to estimate Norwalk-like virus contamination of oysters implicated in an outbreak. Int J Food Microbiol 87:107–112. https://doi.org/10.1016/S0168-1605(03)00058-8

    Article  PubMed  Google Scholar 

  21. Ng TL, Chan PP, Phua TH, Loh JP, Yip R, Wong C et al (2005) Oyster-associated outbreaks of norovirus gastroenteritis in Singapore. J Infect 51:413–418. https://doi.org/10.1016/j.jinf.2004.11.003

    Article  CAS  PubMed  Google Scholar 

  22. Le Guyader FS, Krol J, Ambert-Balay K, Ruvoen-Clouet N, Desaubliaux B, Parnaudeau S et al (2010) Comprehensive analysis of a norovirus-associated gastroenteritis outbreak, from the environment to the consumer. J Clin Microbiol 48:915–920. https://doi.org/10.1128/JCM.01664-09

    Article  PubMed  PubMed Central  Google Scholar 

  23. Lunestad BT, Maage A, Roiha IS, Myrmel M, Svanevik CS, Duinker A (2016) An outbreak of norovirus infection from shellfish soup due to unforeseen insufficient heating during preparation. Food Environ Virol 8:231–234. https://doi.org/10.1007/s12560-016-9245-5

    Article  PubMed  Google Scholar 

  24. Iritani N, Kaida A, Abe N, Kubo H, Sekiguchi J, Yamamoto SP et al (2014) Detection and genetic characterization of human enteric viruses in oyster-associated gastroenteritis outbreaks between 2001 and 2012 in Osaka City. Japan J Med Virol 86:2019–2025

    Article  Google Scholar 

  25. Le Guyader F, Haugarreau L, Miossec L, Dubois E, Pommepuy M (2000) Three-year study to assess human enteric viruses in shellfish. Appl Environ Microbiol 66:3241–3248. https://doi.org/10.1128/AEM.66.8.3241-3248.2000

    Article  PubMed  PubMed Central  Google Scholar 

  26. Ming HX, Fan JF, Wu LJ, Liang YB (2013) Prevalence of human enteric viruses and a potential indicator of contamination in shellfish in China. J Food Saf 33:209–214. https://doi.org/10.1111/jfs.12041

    Article  Google Scholar 

  27. de Farias MF, de Almeida R-B, de Carvalho FCT, Silva CM, dos Reis EMF, Costa RA et al (2010) Condições Microbiológicas De Tagelus Plebeius (Lightfoot, 1786) (Mollusca: Bivalvia: Solecurtidae) E Da Água No Estuário Do Rio Ceará, Em Fortaleza - CE. Bol Do Inst Pesca 36:135–142

    Google Scholar 

  28. Ramos RJ, Pereira MA, Miotto LA, de Faria LFB, Silveira Junior N, Vieira CRW (2010) Microrganismos indicadores de qualidade higiênico-sanitária em ostras (Crassostrea gigas) e águas salinas de fazendas marinhas localizadas na Baía Sul da Ilha de Santa Catarina. Brasil Rev Do Inst Adolfo Lutz 69:29–37

    Google Scholar 

  29. Sande D, Melo TA, Oliveira GSA, Barreto L, Talbot T, Boehs G et al (2010) Prospecção de moluscos bivalves no estudo da poluição dos rios Cachoeira e Santana em Ilhéus, Bahia, Brasil. Brazilian J Vet Res Anim Sci 47:190–196

    Article  Google Scholar 

  30. da Silveira MA, Leão MVP, dos Santos SSF, Jorge AOC, Gonçalves CR, Qualidade sanitária da água e de bivalves Iphigenia brasiliensis (Lamarck, (1818) na praia do Jabaquara, Paraty. RJ Rev Biociências 2011:17

    Google Scholar 

  31. Barbieri E, Bondioli AC, Woiciechovski E, Zapotoski SMK (2012) Microbiology quality of the oysters cultivation water marketed in Cananeia-SP. Brazil O Mundo Da Saúde 36:541–547

    Article  Google Scholar 

  32. Doi SA, de Cardoso Oliveira AJF, Barbieri E (2015) Determinação de coliformes na água e no tecido mole das ostras extraídas em Cananéia, São Paulo. Brasil Eng Sanit e Ambient 20:111–118. https://doi.org/10.1590/S1413-41522015020000125658

    Article  CAS  Google Scholar 

  33. Sincero TCM, Levin DB, Simões CMO, Barardi CRM (2006) Detection of hepatitis A virus (HAV) in oysters (Crassostrea gigas). Water Res 40:895–902

    Article  CAS  Google Scholar 

  34. Rigotto C, Victoria M, Moresco V, Kolesnikovas CK, Corrêa AA, Souza DSM et al (2010) Assessment of adenovirus, hepatitis A virus and rotavirus presence in environmental samples in Florianopolis. South Brazil J Appl Microbiol 109:1979–1987

    Article  CAS  Google Scholar 

  35. Keller R, Justino JF, Cassini ST (2013) Assessment of water and seafood microbiology quality in a mangrove region in Vitória. Brazil J Water Health 11:573–580

    Article  CAS  Google Scholar 

  36. Leal DAG, Souza DSM, Caumo KS, Fongaro G, Panatieri LF, Durigan M et al (2018) Genotypic characterization and assessment of infectivity of human waterborne pathogens recovered from oysters and estuarine waters in Brazil. Water Res 137:273–280

    Article  CAS  Google Scholar 

  37. Brake F, Ross T, Holds G, Kiermeier A, McLeod C (2014) A survey of Australian oysters for the presence of human noroviruses. Food Microbiol 44:264–270. https://doi.org/10.1016/j.fm.2014.06.012

    Article  CAS  PubMed  Google Scholar 

  38. da Silva Luz I, Miagostovich MP. Norovírus em alimentos. Vigilância Sanitária Em Debate Soc Ciência Tecnol (Health Surveill under Debate Soc Sci Technol Em Debate 2017;5:100–15.

  39. Lodder-Verschoor F, de Roda Husman AM, Van Den Berg H, Stein A, van Pelt-Heerschap HML, Van der Poel WHM (2005) Year-round screening of noncommercial and commercial oysters for the presence of human pathogenic viruses. J Food Prot 68:1853–1859

    Article  CAS  Google Scholar 

  40. FDA. FDA 2007.

  41. ISO. ISO 15216–1, 2017. n.d.

  42. Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193

    Article  Google Scholar 

  43. del Favero JM, Dias JF (2015) Juvenile fish use of the shallow zone of beaches of the Cananéia-Iguape coastal system, southeastern Brazil. Brazilian J Oceanogr 63:103–114

    Article  Google Scholar 

  44. De Oliveira FC, Hanazaki N (2011) Ethnobotany and ecological perspectives on the management and use of plant species for a traditional fishing trap, southern coast of São Paulo. Brazil J Environ Manage 92:1783–1792. https://doi.org/10.1016/j.jenvman.2011.02.002

    Article  PubMed  Google Scholar 

  45. Tse H, Chan W-M, Tsoi H-W, Fan RYY, Lau CCY, Lau SKP et al (2011) Rediscovery and genomic characterization of bovine astroviruses. J Gen Virol 92:1888–1898

    Article  CAS  Google Scholar 

  46. Terio V, Martella V, Moschidou P, Di Pinto P, Tantillo G, Buonavoglia C (2010) Norovirus in retail shellfish. Food Microbiol 27:29–32. https://doi.org/10.1016/j.fm.2009.07.005

    Article  CAS  PubMed  Google Scholar 

  47. Yuen LKW, Catton MG, Cox BJ, Wright PJ, Marshall JA (2001) Heminested multiplex reverse transcription-PCR for detection and differentiation of Norwalk-like virus genogroups 1 and 2 in fecal samples. J Clin Microbiol 39:2690–2694. https://doi.org/10.1128/JCM.39.7.2690-2694.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  Google Scholar 

  49. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  50. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser., vol. 41, [London]: Information Retrieval Ltd., c1979-c2000.; 1999, p. 95–8.

  51. Campanella JJ, Bitincka L, Smalley J (2003) MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 4:1–4

    Article  Google Scholar 

  52. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013;30:2725–9.

  53. Yamashita T, Kobayashi S, Sakae K, Nakata S, Chiba S, Ishihara Y et al (1991) Isolation of cytopathic small round viruses with BS-C-1 cells from patients with gastroenteritis. J Infect Dis 164:954–957. https://doi.org/10.1093/infdis/164.5.954

    Article  CAS  PubMed  Google Scholar 

  54. Elamri DE, Aouni M, Parnaudeau S, Le Guyader FS (2006) Detection of human enteric viruses in shellfish collected in Tunisia. Lett Appl Microbiol 43:399–404. https://doi.org/10.1111/j.1472-765X.2006.01978.x

    Article  CAS  PubMed  Google Scholar 

  55. Gabrieli R, Macaluso A, Lanni L, Saccares S, Di Giamberardino F, Cencioni B et al (2007) Enteric viruses in molluscan shellfish. New Microbiol 30:471–475

    PubMed  Google Scholar 

  56. Le Guyader FS, Le Saux JC, Ambert-Balay K, Krol J, Serais O, Parnaudeau S et al (2008) Aichi virus, norovirus, astrovirus, enterovirus, and rotavirus involved in clinical cases from a French oyster-related gastroenteritis outbreak. J Clin Microbiol 46:4011–4017. https://doi.org/10.1128/JCM.01044-08

    Article  PubMed  PubMed Central  Google Scholar 

  57. Miagostovich MP, Ferreira FFM, Guimarães FR, Fumian TM, Diniz-Mendes L, Luz SLB et al (2008) Molecular detection and characterization of gastroenteritis viruses occurring naturally in the stream waters of Manaus, central Amazonia. Brazil Appl Environ Microbiol 74:375–382

    Article  CAS  Google Scholar 

  58. Fumian TM, Vieira CB, Leite JPG, Miagostovich MP (2013) Assessment of burden of virus agents in an urban sewage treatment plant in Rio de Janeiro. Brazil J Water Health 11:110–119

    Article  CAS  Google Scholar 

  59. Nuñez LFN, Parra SHS, Carranza C, Astolfi-Ferreira CS, Buim MR, Ferreira AJP (2016) Detection and molecular characterization of chicken astrovirus associated with chicks that have an unusual condition known as “white chicks” in Brazil. Poult Sci 95:1262–1270

    Article  Google Scholar 

  60. Siqueira JAM, de Souza OD, de Carvalho TCN, Portal TM, Justino MCA, da Silva LD et al (2017) Astrovirus infection in hospitalized children: molecular, clinical and epidemiological features. J Clin Virol 94:79–85

    Article  CAS  Google Scholar 

  61. Alves CDBT, Budaszewski RF, Torikachvili M, Streck AF, Weber MN, Cibulski SP et al (2018) Detection and genetic characterization of Mamastrovirus 5 from Brazilian dogs. Brazilian J Microbiol 49:575–583

    Article  CAS  Google Scholar 

  62. Gularte JS, Girardi V, Demoliner M, de Souza FG, Filippi M, Eisen AKA et al (2019) Human mastadenovirus in water, sediment, sea surface microlayer, and bivalve mollusk from southern Brazilian beaches. Mar Pollut Bull 142:335–349

    Article  CAS  Google Scholar 

  63. Gentry J, Vinjé J, Guadagnoli D, Lipp EK (2009) Norovirus distribution within an estuarine environment. Appl Environ Microbiol 75:5474–5480. https://doi.org/10.1128/AEM.00111-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Boxman ILA, Tilburg JJHC, te Loeke NAJM, Vennema H, Jonker K, de Boer E et al (2006) Detection of noroviruses in shellfish in the Netherlands. Int J Food Microbiol 108:391–396. https://doi.org/10.1016/j.ijfoodmicro.2006.01.002

    Article  CAS  PubMed  Google Scholar 

  65. Croci L, Losio MN, Suffredini E, Pavoni E, Di Pasquale S, Fallacara F et al (2007) Assessment of human enteric viruses in shellfish from the northern Adriatic sea. Int J Food Microbiol 114:252–257. https://doi.org/10.1016/j.ijfoodmicro.2006.09.015

    Article  PubMed  Google Scholar 

  66. Lees D (2000) Viruses and bivalve shellfish. Int J Food Microbiol 59:81–116. https://doi.org/10.1016/S0168-1605(00)00248-8

    Article  CAS  PubMed  Google Scholar 

  67. Atmar RL (2010) Noroviruses: state of the art. Food Environ Virol 2:117–126

    Article  Google Scholar 

  68. Le Saux JC, Serais O, Krol J, Parnaudeau S, Salvagnac P, Delmas G, et al. Evidence of the presence of viral contamination in shellfish after short rainfall events. J Shellfish Res Open Access Version Http//Archier Ifremer Fr/Doc/00066/17736 2009.

  69. Bigoraj E, Kwit E, Chrobocińska M, Rzeżutka A (2014) Occurrence of norovirus and hepatitis A virus in wild mussels collected from the Baltic Sea. Food Environ Virol 6:207–212. https://doi.org/10.1007/s12560-014-9153-5

    Article  CAS  PubMed  Google Scholar 

  70. Moresco V, Viancelli A, Nascimento MA, Souza DSM, Ramos APD, Garcia LAT et al (2012) Microbiological and physicochemical analysis of the coastal waters of Southern Brazil. Mar Pollut Bull 64:40–48

    Article  CAS  Google Scholar 

  71. Ferro de Godoy D, Andriolo A, de Fatima Filla G. The influence of environmental variables on estuarine dolphins (Sotalia guianensis) spatial distribution and habitat used in the Estuarine Lagunar Complex of Cananéia, southeastern Brazil. Ocean Coast Manag 2015;106:68–76. https://doi.org/10.1016/j.ocecoaman.2015.01.013.

  72. Keller R, Pratte-Santos R, Scarpati K, Martins SA, Loss SM, Fumian TM et al (2019) Surveillance of enteric viruses and thermotolerant coliforms in surface water and bivalves from a mangrove estuary in southeastern Brazil. Food Environ Virol 11:288–296

    Article  Google Scholar 

  73. Corrêa A de A, Rigotto C, Moresco V, Kleemann CR, Teixeira AL, Poli CR, et al. The depuration dynamics of oysters (Crassostrea gigas) artificially contaminated with hepatitis A virus and human adenovirus. Mem Inst Oswaldo Cruz 2012;107:11–7.

  74. Souza DSM, Piazza RS, Pilotto MR, do Nascimento M de A, Moresco V, Taniguchi S, et al. Virus, protozoa and organic compounds decay in depurated oysters. Int J Food Microbiol 2013;167:337–45.

  75. Sobral Marques Souza D, Miura T, Le Mennec C, Barardi CRM, Le Guyader FS. Retention of rotavirus infectivity in mussels heated by using the French recipe Moules Marinières. J Food Prot 2015;78:2064–9.

  76. Souza DSM, Ramos APD, Nunes FF, Moresco V, Taniguchi S, Leal DAG et al (2012) Evaluation of tropical water sources and mollusks in southern Brazil using microbiological, biochemical, and chemical parameters. Ecotoxicol Environ Saf 76:153–161

    Article  CAS  Google Scholar 

  77. Guarines KM, Mendes RPG, Cordeiro MT, Miagostovich MP, Gil L, Green KY, et al. Absence of norovirus contamination in shellfish harvested and commercialized in the Northeast coast of Brazil. Brazilian J Med Biol Res 2020;53.

  78. Sarmento SK, Guerra CR, Malta FC, Coutinho R, Miagostovich MP, Fumian TM. Human norovirus detection in bivalve shellfish in Brazil and evaluation of viral infectivity using PMA treatment. Mar Pollut Bull 2020;157:111315.

  79. 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. https://doi.org/10.1128/JCM.00279-06

    Article  CAS  PubMed  Google Scholar 

  80. Morillo SG, Audrey C, Carmona R de CC, Timenetsky M do CST. Identification and molecular characterization of norovirus in São Paulo State, Brazil. Brazilian J Microbiol 2008;39:619–22.

  81. da Silva PT, Peiró JR, Mendes LCN, Ludwig LF, de Oliveira-Filho EF, Bucardo F et al (2016) Human norovirus infection in Latin America. J Clin Virol 78:111–119. https://doi.org/10.1016/j.jcv.2016.03.016

    Article  Google Scholar 

  82. Gallimore CI, Iturriza-Gomara M, Xerry J, Adigwe J, Gray JJ (2007) Inter-seasonal diversity of norovirus genotypes: emergence and selection of virus variants. Arch Virol 152:1295–1303. https://doi.org/10.1007/s00705-007-0954-9

    Article  CAS  PubMed  Google Scholar 

  83. Vinje J, Koopmans MPG (1996) Molecular detection and epidemiology of small round-structured viruses in outbreaks of gastroenteritis in the Netherlands. J Infect Dis 174:610–615

    Article  CAS  Google Scholar 

  84. Lopman B, Vennema H, Kohli E, Pothier P, Sanchez A, Negredo A et al (2004) Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet 363:682–688

    Article  Google Scholar 

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Acknowledgements

The authors want to thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the doctoral scholarship and to the Laboratory of Molecular and Cellular Biology of Microorganisms, under the responsibility of Dr. Sandro Roberto Valentini and Prof. Dr. Cleslei Fernando Zanelli, from the Faculty of Pharmaceutical Sciences of the Paulista State University “Julio de Mesquita Filho,” Araraquara Campus for the sequencing of samples.

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Authors and Affiliations

  1. Faculdade de Zootecnia E Engenharia de Alimentos, Universidade de São Paulo, Duque de Caxias Norte, 225, Pirassununga, SP, 13635-900, Brazil

    Andrea Vasquez-García, Julian Eduardo Mejia-Ballesteros, Silvia Helena Seraphin de Godoy, Ricardo Luiz Moro de Sousa & Andrezza Maria Fernandes

  2. Escuela de Ciencias Básicas Tecnología E Ingeniería, Universidad Nacional Abierta Y a Distancia, 763532, Palmira, Colombia

    Andrea Vasquez-García

  3. Escuela de Ciencias Agrarias Pecuarias Y del Medio Ambiente,, Universidad Nacional Abierta Y a Distancia, 763532, Palmira, Colombia

    Julian Eduardo Mejia-Ballesteros

  4. Instituto de Pesca - APTA-SAA/SP. Prof, Besnard s/n, Cananéia, SP, 11990-000, Brazil

    Edison Barbieri

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Contributions

AVG and AMF conceived the study and wrote the manuscript; AMF and RLMS designed the study protocol; JEMB and SHSG performed the microbiology experiments and interpretation of the data; EB assessed and acquired samples of mussels and oysters. All authors contributed to the analysis and interpretation of the data and revised the manuscript.

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Correspondence to Andrezza Maria Fernandes.

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Vasquez-García, A., Mejia-Ballesteros, J.E., de Godoy, S.H.S. et al. Norovirus GII and astrovirus in shellfish from a mangrove region in Cananéia, Brazil: molecular detection and characterization. Braz J Microbiol 53, 317–326 (2022). https://doi.org/10.1007/s42770-021-00631-y

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