The Impact of the Extreme Amazonian Flood Season on the Incidence of Viral Gastroenteritis Cases
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During the Amazonian flood season in 2012, the Negro River reached its highest level in 110 years, submerging residential and commercial areas which appeared associated with an elevation in the observed gastroenteritis cases in the city of Manaus. The aim of this study was to evaluate the microbiological water quality of the Negro River basin during this extreme flood to investigate this apparent association between the illness cases and the population exposed to the contaminated waters. Forty water samples were collected and analysed for classic and emerging enteric viruses. Human adenoviruses, group A rotaviruses and genogroup II noroviruses were detected in 100, 77.5 and 27.5% of the samples, respectively, in concentrations of 103–106 GC/L. All samples were compliant with local bacteriological standards. HAdV2 and 41 and RVA G2, P, and P were characterised. Astroviruses, sapoviruses, genogroup IV noroviruses, klasseviruses, bocaviruses and aichiviruses were not detected. Statistical analyses showed correlations between river stage level and reported gastroenteritis cases and, also, significant differences between virus concentrations during this extreme event when compared with normal dry seasons and previous flood seasons of the Negro River. These findings suggest an association between the extreme flood experienced and gastrointestinal cases in the affected areas providing circumstantial evidence of causality between the elevations in enteric viruses in surface waters and reported illness.
KeywordsAmazon Enteric viruses Flood Negro River qPCR
This work was funded by Viroclime project (www.viroclime.org) as part of the European Union 7th Framework Programme for Research, contract number 243923. We thank the PDTIS DNA Sequence Platform staff at FIOCRUZ-RJ for technical support in sequencing reactions and the FIOCRUZ-Manaus team for helping with samplings. This research work is within the scope of the activities of FIOCRUZ as a collaborating centre of PAHO/WHO of Public and Environmental Health.
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Conflict of interest
The authors declare that they have no conflict of interest.
- Ahmed, M. U., Urasawa, S., Taniguchi, K., Urasawa, T., Kobayashi, N., Wakasugi, F., et al. (1991). Analysis of human rotavirus strains prevailing in Bangladesh in relation to nationwide floods brought by the 1988 monsoon. Journal of Clinical Microbiology, 29(10), 2273–2279.PubMedPubMedCentralGoogle Scholar
- Amaral, M. S., Estevam, G. K., Penatti, M., Lafontaine, R., Lima, I. C., Spada, P. K., et al. (2015). The prevalence of norovirus, astrovirus and adenovirus infections among hospitalised children with acute gastroenteritis in Porto Velho, state of Rondônia, western Brazilian Amazon. Memórias do Instituto Oswaldo Cruz, 110(2), 215–221.CrossRefPubMedPubMedCentralGoogle Scholar
- Bofill-Mas, S., Rusiñol, M., Fernandez-Cassi, X., Carratalà, A., Hundesa, A., & Girones, R. (2013). Quantification of human and animal viruses to differentiate the origin of the fecal contamination present in environmental samples. Biomed Research International, 2013, 192089.CrossRefPubMedPubMedCentralGoogle Scholar
- Calgua, B., Fumian, T., Rusiñol, M., Rodriguez-Manzano, J., Mbayed, V. A., Bofill-Mas, S., et al. (2013). Detection and quantification of classic and emerging viruses by skimmed-milk flocculation and PCR in river water from two geographical areas. Water Research, 47(8), 2797–2810.CrossRefPubMedGoogle Scholar
- Carvalho-Costa, F. A., Mello Volotão, E., de Assis, R. M., Fialho, A. M., de Andrade, J. D. S., Rocha, L. N., et al. (2011). Laboratory-based rotavirus surveillance during the introduction of a vaccination program, Brazil, 2005-2009. The Pediatric Infectious Disease Journal, 30(1 Suppl), S35–S41.CrossRefPubMedGoogle Scholar
- CONAMA—National Environment Council (Conselho Nacional do Meio Ambiente). (2000). Ministério do Meio Ambiente. Resolução 274 de 29 de novembro de 2000. Diário Oficial da República Federativa do Brasil, Poder Executivo, Brasília, DF.Google Scholar
- da Silva Assis, M. R., Vieira, C. B., Fioretti, J. M., Rocha, M. S., de Almeida, P. I., Miagostovich, M. P., et al. (2016). Detection and molecular characterization of gemycircularvirus from environmental samples in Brazil. Food and Environmental Virology, 8, 305–309. In press.CrossRefPubMedGoogle Scholar
- Fumian, T. M., Leite, J. P., Rose, T. L., Prado, T., & Miagostovich, M. P. (2011). One year environmental surveillance of rotavirus specie A (RVA) genotypes in circulation after the introduction of the Rotarix® vaccine in Rio de Janeiro, Brazil. Water Research, 45(17), 5755–5763.CrossRefPubMedGoogle Scholar
- Gómez, M. M., da Silva, M. F., Zeller, M., Heylen, E., Matthijnssens, J., Ichihara, M. Y., et al. (2013). Phylogenetic analysis of G1P group A rotavirus strains detected in Northeast Brazilian children fully vaccinated with Rotarix™. Infection, Genetics and Evolution, 19, 395–402.CrossRefPubMedGoogle Scholar
- Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.Google Scholar
- Hernandez, J. D., da Silva, L. D., Sousa Junior, E. C., de Lucena, M. S., da Soares, L., Mascarenhas, J. D., et al. (2016). Analysis of uncommon norovirus recombinants from Manaus, Amazon region, Brazil: GII.P22/GII.5, GII.P7/GII.6 and GII.Pg/GII.1. Infection, Genetics and Evolution, 39, 365–371.CrossRefPubMedGoogle Scholar
- Hernroth, B. E., Conden-Hansson, A. C., Rehnstam-Holm, A. S., Girones, R., & Allard, A. K. (2002). Environmental factors influencing human viral pathogens and their potential indicator organisms in the blue mussel, Mytilus edulis: The first Scandinavian report. Applied and Environmental Microbiology, 68(9), 4523–4533.CrossRefPubMedPubMedCentralGoogle Scholar
- IBGE—The Brazilian Institute of Geography and Statistics (Instituto Brasileiro de Geografia e Estatística). (2015). http://www.cidades.ibge.gov.br/xtras/perfil.php?codmun=130260. Accessed 10 May 2015
- Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., et al. (2003). Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of Clinical Microbiology, 41(4), 1548–1557.CrossRefPubMedPubMedCentralGoogle Scholar
- Kantola, K., Sadeghi, M., Antikainen, J., Kirveskari, J., Delwart, E., Hedman, K., et al. (2010). Real-time quantitative PCR detection of four human bocaviruses. Journal of Clinical Microbiology, 48(11), 4044–4050. Erratum in (2011). Journal of Clinical Microbiology, 48(11), 4044–4050. Erratum in (2011) Journal of Clinical Microbiology 49, 4029.CrossRefPubMedPubMedCentralGoogle Scholar
- Kitajima, M., Hata, A., Yamashita, T., Haramoto, E., Minagawa, H., & Katayama, H. (2013). Development of a reverse transcription-quantitative PCR system for detection and genotyping of aichi viruses in clinical and environmental samples. Applied and Environmental Microbiology, 79(13), 3952–3958.CrossRefPubMedPubMedCentralGoogle Scholar
- Maestri, R. P., Kaiano, J. H., Neri, D. L., Soares, L. D. S., Guerra, S. D. F., Oliveira, D. D. S., et al. (2012). Phylogenetic analysis of probable non-human genes of group A rotaviruses isolated from children with acute gastroenteritis in Belém, Brazil. Journal of Medical Virology, 84(12), 1993–2002.CrossRefPubMedGoogle Scholar
- MDDA—Brazilian Program of Monitoring Acute Diarrheal Diseases (Programa Brasileiro de Monitorização das Doenças Diarreicas Agudas). (2015). Ministério da Saúde, Brasília, DFGoogle Scholar
- Melo, T. (2014). http://g1.globo.com/am/amazonas/noticia/2013/05/manaus-tera-plano-de-enfrentamento-de-doencas-causadas-pela-cheia.html Accessed 10 May 2014.
- Miagostovich, M. P., Ferreira, F. F. M., Guimarães, F. R., Fumian, T. M., Diniz-Mendes, L., Luz, S. L. B., et al. (2008). Molecular detection and characterization of gastroenteritis viruses occurring naturally in the stream waters of Manaus, Central Amazonia, Brazil. Applied and Environmental Microbiology, 74(2), 375–382.CrossRefPubMedGoogle Scholar
- Port of Manaus (Porto de Manaus). (2015). http://www.portodemanaus.com.br/?pagina=niveis-maximo-minimo-do-rio-negro Accessed 10 May 2015.
- PROSAMIM—Social and Environmental Program for the Igarapés in Manaus (Programa Ambiental e Social dos Igarapés de Manaus). (2004). Relatório de Impacto Ambiental—RIMA. Manaus, Igarapé do Educandos. Governo do Estado do Amazonas, Secretaria de Estado de Infra-estrutura e Concremat Engenharia: Amazonas, Brasil.Google Scholar
- PROSAMIM—Social and Environmental Program for the Igarapés in Manaus (Programa Ambiental e Social dos Igarapés de Manaus). (2012). PROSAMIM III—Igarapé São Raimundo Projeto Executivo. Igarapé São Raimundo, RIMA—Relatório de Impacto Ambiental—REV. 01; Governo do Estado do Amazonas, Secretaria de Estado de Infra-estrutura, Unidade de Gerenciamento de Programa Social e Ambiental dos Igarapés de Manaus (UGPI) e Concremat Engenharia: Amazonas, Brasil.Google Scholar
- Rusiñol, M., Fernandez-Cassi, X., Timoneda, N., Carratalà, A., Abril, J. F., Silvera, C., et al. (2015). Evidence of viral dissemination and seasonality in a Mediterranean river catchment: Implications for water pollution management. Journal of Environmental Management, 159, 58–67.CrossRefPubMedGoogle Scholar
- Schwartz, B. S., Harris, J. B., Khan, A. I., Larocque, R. C., Sack, D. A., Malek, M. A., et al. (2006). Diarrheal epidemics in Dhaka, Bagladesh, during three consecutive floods: 1988, 1998, and 2004. American Journal of Tropical Medicine and Hygiene, 74(6), 1067–1073.PubMedPubMedCentralGoogle Scholar
- Silva, L. D., Rodrigues, E. L., Lucena, M. S., Lima, I. C., Oliveira, D. D. S., Soares, L. S., et al. (2013). Detection of the pandemic norovirus variant GII.4 Sydney 2012 in Rio Branco, state of Acre, northern Brazil. Memórias do Instituto Oswaldo Cruz, 108(8), 1068–1070.CrossRefPubMedPubMedCentralGoogle Scholar
- Siqueira, J. A., Linhares, A. D. C., Gonçalves, M. D. S., Carvalho, T. C., Justino, M. C., Mascarenhas, J. D., et al. (2013). Group A rotavirus and norovirus display sharply distinct seasonal profiles in Belém, northern Brazil. Memórias do Instituto Oswaldo Cruz, 108(5), 661–664.CrossRefPubMedPubMedCentralGoogle Scholar
- Trujillo, A. A., McCaustland, K. A., Zheng, D. P., Hadley, L. A., Vaughn, G., Adams, S. M., et al. (2006). Use of TaqMan real-time reverse transcription-PCR for rapid detection, quantification, and typing of norovirus. Journal of Clinical Microbiology, 44(4), 1405–1412.CrossRefPubMedPubMedCentralGoogle Scholar
- WHO—World Health Organization. (2009). WHO/IVB/08.17—Manual of rotavirus detection and characterization methods (pp. 59–99). Geneva: World Health Organization, Department of Immunization, Vaccines and Biologicals.Google Scholar
- Yard, E. E., Murphy, M. W., Schneeberger, C., Narayanan, J., Hoo, E., Freiman, A., et al. (2014). Microbial and chemical contamination during and after flooding in the Ohio River-Kentucky. Journal of Environmental Science and Health. Part A, Toxic/Hazardous Substances & Environmental Engineering, 49(11), 1236–1243.Google Scholar