Quantification and molecular characterization of enteric viruses detected in effluents from two hospital wastewater treatment plants

Water Research

Volumn 45, Issue 3, 2011, Pages 1287-1297

  Prado, Tatiana ^a   Silva, Dalton M ^a   Guilayn, Wilma C ^a   Rose, Tatiana L ^a   Gaspar, Ana Maria C ^a   Miagostovich, Marize P ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Activated sludge; Anaerobic filters; Enteric viruses; Hospital wastewater; Molecular characterization; Upflow anaerobic sludge blanket (UASB)

Indexed keywords

ACTIVATED SLUDGE PROCESS; FILTERS (FOR FLUIDS); FILTRATION; HOSPITALS; PLANTS (BOTANY); POLYMERASE CHAIN REACTION; SEWAGE; SEWAGE PUMPING PLANTS; VIRUSES; WASTEWATER TREATMENT; WATER TREATMENT PLANTS;

ACTIVATED SLUDGE; ANAEROBIC FILTERS; ENTERIC VIRUS; HOSPITAL WASTEWATER; MOLECULAR CHARACTERIZATION; UPFLOW ANAEROBIC SLUDGE BLANKETS;

EFFLUENTS;

ACTIVATED SLUDGE; CHLORINATION; DETECTION METHOD; EFFLUENT; GASTROENTERITIS; HEPATITIS; HOSPITAL SECTOR; MOLECULAR ANALYSIS; POLLUTION POLICY; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; SEWAGE TREATMENT; VIRUS;

ACTIVATED SLUDGE; ACUTE GASTROENTERITIS; AMPLICON; ANAEROBIC FILTER; ARTICLE; BRAZIL; CHLORINATION; CONTROLLED STUDY; EFFLUENT; ENTERIC VIRUS; HEALTH CARE FACILITY; HEPATITIS; HEPATITIS A VIRUS; HUMAN ADENOVIRUS; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLLUTION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAVIRUS; SEWAGE DISPOSAL; SEWAGE TREATMENT; SLUDGE BLANKET REACTOR; VIRUS DETECTION; VIRUS GENOME; VIRUS LOAD; WASTE WATER TREATMENT PLANT;

BRAZIL; RIO DE JANEIRO [BRAZIL];

HEPATITIS A VIRUS; HUMAN ADENOVIRUS; NOROVIRUS; ROTAVIRUS A;

EID: 78650582022     PISSN: 00431354     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.watres.2010.10.012     Document Type: Article

References (49)

1. Allard A., Albinsson B., Wadell G. Rapid typing of human adenoviruses by a general PCR combined with restriction endonuclease analysis. J. Clin. Microbiol. 2001, 39:498-505.
2. Standard Methods for the Examination Water and Wastewater 1998, American Public Health Association, --, APHAAPHA, American Public Health Association, Washington, DC. twentieth ed.
3. Barrella K.M., Garrafa P., Monezi T.A., Hársi C.M., Salvi C., Violante P.A.B.C., Mehnert D.U. Longitudinal study on occurrence of adenoviruses and hepatitis A virus in raw domestic sewage in the city of Limeira, São Paulo. Braz. J. Microbiol. 2009, 40:102-107.
4. Bastien P., Procop G.W., Reischl U. Quantitative Real-Time PCR is not more sensitive than "conventional" PCR. J. Clin. Microbiol. 2008, 46:1897-1900.
5. Bofill-Mas S., Gimenez N.A., Casares P.C., Hundesa A., Manzano J.R., Allard A., Calvo M., Girones R. Quantification and stability of human adenoviruses and polyomavirus JCPyV in wastewater matrices. Appl. Environ. Microbiol. 2006, 72:7894-7896.
6. Bosch A., Guix S., Sano D., Pintó R.M. New tools for the study and direct surveillance of viral pathogens in water. Curr. Opin. Biotechnol. 2008, 19(3):295-301.
7. Boxman I.L.A., Tilburg J.J.H.C., Te Loeke N.A.J.M., Vennema H., Jonker K., Boer E., Koopmans M. Detection of noroviruses in shellfish in the Netherlands. Int. J. Food Microbiol. 2006, 108:391-396.
8. Cantera J.L., Chen W., Yates M.V. Detection of infective poliovirus by a simple, rapid, and sensitive flow cytometry method based on fluorescence resonance energy transfer technology. Appl. Environ. Microbiol. 2010, 76:584-588.
9. Carducci A., Morici P., Pizzi F., Battistini R., Rovini E., Verani M. Study of the viral removal efficiency in a urban wastewater treatment plant. Water Sci. Technol. 2008, 58:893-897.
10. Cromeans T.L., Kahler A.M., Hill V.R. Inactivation of adenoviruses, enteroviruses, and murine norovirus in water by free chlorine and monochloramine. Appl. Environ. Microbiol. 2010, 76(4):1028-1033.
11. Costa-Mattioli M., Ferré V., Monpoeho S., Garcia L., Colina R., Billaudel S., Vega I., Perez-Bercoff R., Cristina J. Genetic variability of hepatitis A virus in South America reveals heterogeneity and co-circulation during epidemic outbreaks. J. Gen. Virol. 2001, 82:2647-2652.
12. De Paula V.S., Baptista M.L., Lampe E., Niel C., Gaspar A.M.C. Characterization of hepatitis A virus isolates from subgenotypes IA and IB in Rio de Janeiro. Braz. J. Med. Virol. 2002, 66:22-27.
13. De Paula V.S., Diniz-Mendes L., Villar L.M., Luz S.L.B., Silva L.A., Jesus M.S., Da Silva N.M.V.S., Gaspar A.M.C. Hepatitis A virus in environmental water samples from the Amazon Basin. Water Res. 2007, 41:1169-1176.
14. Emmanuel E., Perrodin Y., Keck G., Blanchard J.M., Vermande P. Ecotoxicological risk assessment of hospital wastewater: a proposed framework for raw effluents discharging into urban sewer network. J. Hazard. Mater. 2005, 117:1-11.
15. Emmanuel E., Pierre M.G., Perrodin Y. Groundwater contamination by microbiological and chemical substances released from hospital wastewater: health risk assessment for drinking water consumers. Environ. Int. 2009, 35:718-726.
16. Espinosa A.C., Mazari-Hiriart M., Espinosa R., Maruri-Avidal L., Méndez E., Arias C.F. Infectivity and genome persistence of rotavirus and astrovirus in groundwater and surface water. Water Res. 2008, 42:2618-2628.
17. Ferreira F.F.M., Guimarães F.R., Fumian T.M., Victoria M., Vieira C.B., Luz S., Shubo T., Leite J.P.G., Miagostovich M.P. Environmental dissemination of group A rotavirus: P-type, G-type and subgroup characterization. Water Sci. Technol. 2009, 60:633-642.
18. Girones R., Ferrús M.A., Alonso J.L., Rodriguez-Manzano J., Calgua B., Corrêa A.B., Hundesa A., Carratala A., Bofill-Mas Molecular detection of pathogens in water - The pros and cons of molecular techniques. Water Res. 2010, 44:4325-4339.
19. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41:95-98.
20. Haramoto E., Katayama H., Oguma K., Ohgaki S. Recovery of naked viral genomes in water by virus concentration methods. J. Virol. Methods 2007, 142:169-173.
21. Haramoto E., Katayama H., Oguma K., Ohgaki S. Quantitative analysis of human enteric adenoviruses in aquatic environments. J. Appl. Microbiol. 2007, 103:2153-2159.
22. Heim A., Ebnet C., Harste G. Pring-Akerblom, P. Rapid and quantitative detection of human adenovirus DNA by real-time PCR. J. Med. Virol. 2003, 70:228-239.
23. Ishiko H., Shimada Y., Konno T., Hayashi A., Ohguchi T., Tagawa Y., Aoki K., Ohno S., Yamazaki S. Novel human adenovirus causing nosocomial epidemic keratoconjunctivitis. J. Clin. Microbiol. 2008, 46(6):2002-2008.
24. Iturriza-Gómara M.I., Wong C., Blome S., Desselberger U., Gray J. Molecular characterization of VP6 genes of human rotavirus isolates, correlation of genogroups with subgroups and evidence of independent segregation. J. Virol. 2002, 76:6596-6601.
25. Katayama H., Shimasaki A., Ohgaki S. Development of a virus concentration method and its Application to detect of Enterovirus and Norwalk virus from Coastal Seawater. Appl. Environ. Microbiol. 2002, 68:1033-1039.
26. Katayama H., Haramoto E., Oguma K., Yamashita H., Tajima A., Nakajima H., Ohgaki S. One-year monthly quantitative survey of noroviruses, enteroviruses, and adenoviruses in wastewater collected from six plants in Japan. Water Res. 2008, 42:1441-1448.
27. Leite J.P.G., Carvalho-Costa F.A., Linhares A.C. Group A rotavirus genotypes and the ongoing Brazilian experience - A Review. Mem. Inst. Oswaldo Cruz 2008, 103(8):745-753.
28. Lim M.Y., Kim J.M., Ko G. Disinfection kinetics of murine norovirus using chlorine and chlorine dioxide. Water Res. 2010, 44:3243-3251.
29. Miagostovich M.P., Ferreira F.F.M., Guimarães F.R., Fumian T.M., Diniz-Mendes L., Luz S.L.B., Silva L.A., Leite J.P.G. Molecular detection and characterization of gastroenteritis viruses occurring naturally in the stream waters of Manaus, Central Amazônia, Brazil. Appl. Environ. Microbiol. 2008, 74:375-382.
30. Otto T.D., Vasconcellos E.A., Gomes L.H.F., Moreira A.S., Degrave W.M., Mendonça-Lima L., Alves-Ferreira M. ChromaPipe: a pipeline for analysis, quality control and management for a DNA sequencing facility. Genet. Mol. Res. 2008, 7:861-871.
31. Ottoson J., Hansen A., Bjorlenius B., Norder H., Stenstrom T.A. Removal of viruses, parasitic protozoa and microbial indicators in conventional and membrane processes in a wastewater pilot plant. Water Res. 2006, 40:1449-1457.
32. Pang X.L., Preiksaitis J.K., Lee B. Multiplex real-time RT-PCR for the detection and quantitation of norovirus genogroups I and II in patients with acute gastroenteritis. J. Clin. Virol. 2005, 33:168-171.
33. Parashar U.D., Gibson C.J., Bresee J.S., Glass R.I. Rotavirus and severe childhood diarrhea. Emerg. Infect. Dis. 2006, 12(2):304-306.
34. Pereira-Filho E., Faria N.R.C., Fialho A.M., Assis R.S., Almeida M.M.S., Rocha M., Galvão M., Santos F.B., Barreto M.L., Leite J.P.G. Adenoviruses associated with acute gastroenteritis in hospitalized and community children up to 5 years old in Rio de Janeiro and Salvador, Brazil. J. Med. Microbiol. 2007, 56:313-319.
35. Petrinca A.R., Donia D., Pierangeli A., Gabrieli A.M., Degener A.M., Bonanni E., Diaco L., Cecchini G., Anastasi P., Divizia M. Presence and environment circulation of enteric viruses in three different wastewater treatment plants. J. Appl. Microbiol. 2009, 106:1608-1617.
36. Prado T., Pereira W.C., Silva D.M., Seki L.M., Carvalho A.P.D., Asensi M.D. Detection of extended-spectrum β-lactamase-producing Klebsiella pneumoniae in effluents and sludge of a hospital sewage treatment plant. Lett. Appl. Microbiol. 2008, 46:136-141.
37. Rezaee A., Ansari M., Khavanin A., Sabzali A., Aryan M.M. Hospital wastewater treatment using an integrated anaerobic aerobic fixed film bioreactor. Am. J. Environ. Sci. 2005, 1(4):259-263.
38. Siebenga J.J., Vennema H., Renckens H., Bruin E., Van der Veer B., Siezen R.J., Koopmans M. Epochal evolution of GGII.4 norovirus capside proteins from 1995 to 2006. J. Virol. 2007, 81:9932-9941.
39. Silva P.C., Vitral C.L., Barcellos C., Kawa H., Gracie R., Rosa M.L.G. Hepatitis A in the city of Rio de Janeiro, Brazil: epidemiological pattern and socio-environmental variables. Cross-analysis of SINAN and population census data 2007, vol. 23. Cad. Saude Publica, Rio de Janeiro, 1553-1564.
40. Tamura K., Dudley J., Nei M., Kumar S. MEGA 4: molecular Evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
41. Tan M., Jiang X. Norovirus-host interaction: implications for disease control and prevention. Expert Rev. Molecular Medicine 2007, 9(19):1-22.
42. Tyrrell S.A., Rippley S.R., Watkins W.D. Inactivation of bacterial and viral indicators in secondary sewage effluents, using chlorine and ozone. Water Res. 1995, 29(11):2483-2490.
43. Victoria M., Carvalho-Costa F.A., Heinemann M.B., Leite J.P., Miagostovich M.P. Prevalence and molecular epidemiology of noroviruses in hospitalized children with acute gastroenteritis in Rio de Janeiro, Brazil, 2004. Pediatr. Infect. Dis. J. 2007, 26:602-606.
44. Victoria M., Guimarães F.R., Fumian T.M., Ferreira F.F.M., Vieira C.B., Shubo T., Leite J.P.G., Miagostovich M.P. One year monitoring of norovirus in a sewage treatment plant in Rio de Janeiro, Brazil. J. Water Health 2009, 8:158-165.
45. Villar L.M., De Paula V.S., Diniz-Mendes L., Guimarães F.R., Ferreira F.F.M., Shubo T.C., Miagostovich M.P., Lampe E., Gaspar A.M.C. Molecular detection of hepatitis A virus in urban sewage in Rio de Janeiro, Brazil. Lett. Appl. Microbiol. 2007, 45:168-173.
46. Vitral C.L., Souto F.J., Gaspar A.M.C. Changing epidemiology of hepatitis A in Brazil: reassessing immunization policy. J. Viral. Hepat. 2008, 15(Suppl. 2):22-25.
47. Wang X.W., Li J., Guo T., Zhen B., Kong Q., Yi B., Li Z., Song N., Jin M., Xiao W., Zhu X., Gu C., Yin J., Wei W., Yao W., Liu C., Li J., Ou G., Wang M., Fang T., Wang G., Qiu Y., Wu H., Chao F., Li J. Concentration and detection of SARS coronavirus in sewage from in XiaoTang Shan Hospital and the 309th Hospital of the Chinese People's liberation army. Water Sci. Technol. 2005, 52(8):213-221.
48. Zeng S.Q., Halkosalo A., Salminen M., Szakal E.D., Puustinen L., Vesikari T. One-step quantitative RT-PCR for the detection of rotavirus in acute gastroenteritis. J. Virol. Methods 2008, 153:238-240.
49. Zhang K., Farahbakhsh K. Removal of native coliphages and coliform bacteria from municipal wastewater by various wastewater treatment processes: implications to water reuse. Water Res. 2007, 41:2816-2824.