Municipal wastewater treatment plants as pathogen removal systems and as a contamination source of noroviruses and Enterococcus faecalis

Journal of Water and Health

Volumn 10, Issue 3, 2012, Pages 380-389

  Cheng, Hui Wen A ^a   Lucy, Frances E ^a   Broaders, Michael A ^a   Mastitsky, Sergey E ^b   Chen, Chien Hsien ^c   Murray, Amanda ^d  

^a Atlantic Technological University Sligo   (Ireland)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c TATUNG UNIVERSITY   (Taiwan)

^d HEALTH SERVICE EXECUTIVE   (Ireland)

Author keywords

Biosolids; Enterococcus faecalis; Enterococcus faecium; Noroviruses; Wastewater

Indexed keywords

ACTIVATED SLUDGE; BACTERIUM; BIOSOLID; DOMESTIC WASTE; HEALTH RISK; PATHOGEN; POLLUTANT REMOVAL; POLLUTANT SOURCE; PUBLIC HEALTH; SEASONAL VARIATION; SPATIAL VARIATION; VIRUS; WASTE DISPOSAL; WASTE FACILITY; WASTEWATER; WATER TREATMENT;

ACTIVATED SLUDGE; ARTICLE; BIOFILM REACTOR; BIOSOLID; CONTROLLED STUDY; EFFLUENT; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; HEALTH HAZARD; IRELAND; NONHUMAN; NOROVIRUS; SEASONAL VARIATION; VIRUS PARTICLE; WASTE WATER MANAGEMENT; WASTE WATER TREATMENT PLANT; WATER CONTAMINATION; WATER QUALITY;

ENTEROCOCCUS FAECALIS; IRELAND; NOROVIRUS; RNA, VIRAL; WASTE DISPOSAL, FLUID; WATER MICROBIOLOGY; WATER PURIFICATION;

IRELAND;

ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; NOROVIRUS;

EID: 84866292800     PISSN: 14778920     EISSN: None     Source Type: Journal    
DOI: 10.2166/wh.2012.138     Document Type: Article

References (47)

1. Anderson, M. J. & Robinson, J. 2003 Generalised discriminant analysis based on distances. Aust. NZ. J. Stat. 45, 301-318. (Pubitemid 37023230)
2. Anderson, M. J. 2005 PERMANOVA: A FORTRAN Computer Program for Permutational Multivariate Analysis of Variance. Department of Statistics, University of Auckland, New Zealand.
3. Borchardt, M. A., Chyou, P. H., DeVries, E. O. & Belongia, E. A. 2003 Septic system density and infectious diarrhea in a defined population of children. Environ. Health Perspectives 111, 742-748. (Pubitemid 36621606)
4. Boxman, I. L. A., Tilburg, J. J. H. C., te Loeke, N. A. J. M., Vennema, H., Jonker, K., de Boer, E. & Koopmans, M. 2006 Detection of norovirus in shellfish in the Netherlands. Int. J. Food Microbiol. 108, 391-396.
5. Caul, E. O. 1996 Viral gastroenteritis: small round structured viruses, caliciviruses and astroviruses. Part I. The clinical and diagnostic perspective. J. Clin. Pathol. 49, 874-880. (Pubitemid 26403154)
6. Cheng, H. W. A., Lucy, F. E., Graczyk, T. K., Broaders, M. A., Tamang, L. & Connolly, M. 2009 Fate of Cryptosporidium parvum and Cryptosporidium hominis oocysts and Giardia duodenalis cysts during secondary wastewater treatments. Parasitol. Res. 105, 689-696.
7. Cheng, H. W. A., Lucy, F. E., Graczyk, T. K., Broaders, M. A. & Mastitsky, S. E. 2011 Municipal wastewater treatment plants as removal systems and environmental sources of humanvirulent microsporidian spores. Parasitol. Res. 109, 595-603.
8. Council of the European Community (CEC) 1991 Council directive 91/271/EEC of 21 May 1991 concerning urban wastewater treatment. Off. J. Eur. Union L. 135, 40-52.
9. Council of the European Community (CEC) 2006a Directive 2006/113/EC of the European Parliament and of the Council of 12 December 2006 on the quality required of shellfish waters (codified version). Off. J. Eur. Union L. 376, 14-20.
10. Council of the European Community (CEC) 2006b Directive 2006/7/EC of the European parliament and of the council of 15 February 2006 concerning the management of bathing water quality and repealing directive 76/160/EEC. Off. J. Eur. Union L. 64, 37-51.
11. Deasy, B. M., Rea, M. C., Fitzgerald, G. F., Cogan, T. M. & Beresford, T. P. 2000 A rapid PCR based method to distinguish between Lactococcus and Enterococcus. Syst. Appl. Microbiol. 23, 510-522. (Pubitemid 32110942)
12. European Antimicrobial Resistance Surveillance Network (EARSNet) 2009 Antimicrobial resistance surveillance in Ireland: Results of invasive enterococcal bacteraemia surveillance. Available from: http://www.hpsc.ie/hpsc/ A-Z/MicrobiologyAntimicrobialResistance/ EuropeanAntimicrobialResistanceSurveillanceSystemEARSS/ ReferenceandEducationalResourceMaterial/EnterococciVRE/ ReferenceandEducationalResourceMaterial/File,4830,en.ppt (accessed 27 June 2012).
13. Food Standards Agency 2000 A Report of the Study of Infectious Intestinal Disease in England. HMSO, London.
14. Gale, P. 2005 Land application of treated sewage sludge: qualifying pathogen risk from consumption of crop. J. Appl. Microbiol. 98, 380-396. (Pubitemid 40188156)
15. Graczyk, T. K., Sunderland, D., Tamang, L., Lucy, F. E. & Breysse, P. N. 2007 Bather density and levels of Cryptosporidium, Giardia, and pathogenic microsporidian spores in recreational bathing water. Parasitol. Res. 101, 1729-1731. (Pubitemid 47524865)
16. Graczyk, T. K., Lucy, F. E., Tamang, L., Mashinsky, Y., Broaders, M. A., Connolly, M. & Cheng, H-W. A. 2009 Propagation of human enteropathogens in constructed horizontal wetlands used for tertiary wastewater treatment. Appl. Environ. Microbiol. 75, 4531-4538.
17. Gray, N. F. 2004 Biology of Wastewater Treatment. Imperial College Press, London.
18. Green, J., Wright, P., Gallimore, C., Mitchell, O., Morgan-Capner, P. & Brown, D. 1998 The role of environmental contamination with small round structured viruses in a hospital outbreak investigated by reverse-transcriptase polymerase chain reaction assay. J. Hospital Infect. 39, 39-45. (Pubitemid 28242982)
19. Green, K., Chanock, M. & Kapikian, A. 2011 Human caliciviruses. In: Fields Virology (D. Knipe, ed.), 4th edition. William and Wilkins Press, Philadelphia, PA. pp. 841-874.
20. Heistad, A., Scott, T., Skaarer, A. M., Seidu, R., Hanssen, J. F. & Stenström, T. A. 2009 Virus removal by unsaturated wastewater filtration: effects of biofilm accumulation and hydrophobicity. Water Sci. Technol. 60, 399-407.
21. HPSC 2010 Health Protection Surveillance Centre annual report 2009. Health Protection Surveillance Centre, Ireland.
22. Hsu, B. M., Chen, C. H., Wan, M. T. & Cheng, H. W. A. 2006 Legionella prevalence in hot spring recreation areas of Taiwan. Water Res. 40, 3267-3273.
23. Hsu, B. M., Chen, C. H., Wan, M. T., Chang, P. J. & Fan, C. W. 2009 Detection and identification of enteroviruses from various drinking water sources in Taiwan. J. Hydrology 365, 134-139.
24. Iwai, M., Hasegawa, S., Obara, M., Nakamura, K., Horimoto, E., Takizawa, T., Kurata, T., Sogen, S. I. & Shiraki, K. 2009 Continuous presence of Noroviruses and Sapoviruses in raw sewage reflects infections among inhabitants of Toyama, Japan (2006 to 2008). Appl. Environ. Microbiol. 75, 1264-1270.
25. Jackson, C. R., Fedorka-Cray, P. J. & Barrett, J. B. 2004 Use of a genus- and species-specific multiplex PCR for identification of enterococci. J. Clin. Microbiol. 42, 3558-3565. (Pubitemid 39045680)
26. Katayama, H., Shimasaki, A. & Shinichiro, S. 2002 Development of a virus concentration method and its application of detection of enterovirus and Norwalk virus from coastal water. Appl. Environ. Microbiol. 68, 1033-1039. (Pubitemid 34205338)
27. Kosek, M., Bern, C. & Guerrant, R. L. 2003 The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull. World Health Organiz. 81, 197-204. (Pubitemid 36372958)
28. Koopmans, M, Vennema, H., Heersma, H., van Strien, E., von Duynhoven, Y., Brown, D., Reacher, M. & Lopman, B. 2003 Early identification of common-source foodborne virus outbreaks in Europe. Emerg. Infect. Dis. 9, 1136-1142. (Pubitemid 37071557)
29. Lindesmith, L. C., Donaldson, E. F., LoBue, A. D., Cannon, J. L., Zheng, D. P., Vinje, V. & Baric, R. S. 2008 Mechanisms of GII.4 norovirus persistence in human populations. PLOS Med. 5, 269-290.
30. Liu, Q., Zhou, Y., Chen, L. & Zheng, X. 2010 Application of MBR for hospital wastewater treatment in China. Desalination 250, 605-608.
31. Lopman, B., Vennema, H., Kohli, E., Pothier, P., Sanchez, A., Negredo, A., Buesa, J., Schreier, E., Reacher, M., Brown, D., Gray, J., Iturriza, M., Gallimore, C., Bottiger, B., Hedlund, K. O., Torven, M., von Bonsdorff, C. H., Maunula, L., Poljsak-Prijatelj, M., Zimsek, J., Reuter, G., Szucs, G., Melegh, B., Svennson, L., van Duijnhoven, Y. & Koopmans, M. 2004 Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet 363, 682-688. (Pubitemid 38296554)
32. Lukasik, J., Scott, T. M., Andryshak, D. & Farrah, S. R. 2000 Influence of salts on virus adsorption to microporous filters. Appl. Environ. Microbiol. 54, 1983-1988.
33. Mathers, C., Boerma, T. & Fat, D. M. 2004 Global Burden of Disease: 2004 Update. World Health Organization, Geneva, Switzerland.
34. Moellering, R. C. 1992 Emergence of enterococcus as a significant pathogen. Clin. Infect. Dis. 14, 1173-1176.
35. Monaghan, S., Smith, D., Wall, B. & O'Leary, G. 2009 Urban Waste Water Discharges in Ireland: A Report for the Years of 2006 and 2007. Environmental Protection Agency, Ireland.
36. Nenonen, N. P., Hannoun, C., Horal, P., Hernroth, B. & Bergstrom, T. 2008 Tracing of Norovirus outbreak strains in mussels collected near sewage effluents. Appl. Environ. Microbiol. 74, 2544-2549. (Pubitemid 351555472)
37. NDSC 2003 National guidelines on the management of outbreaks of Norovirus infection in healthcare settings. Annual report of the National Disease Surveillance Centre. National Disease Surveillance Centre, Dublin.
38. Rice, W. R. 1989 Analyzing tables of statistical tests. Evolution 43, 223-225.
39. Rimhanen-Finne, R., Vourinen, A., Marmo, S., Malmbreg, S. & Hanninen, M. L. 2004 Comparative analysis of Cryptosporidium and Giardia and indicator bacteria during sewage sludge hygienization in various composting processes. Lett. Appl. Microbiol. 38, 301-305. (Pubitemid 38445388)
40. Simmons, F. J., Kuo, D. W. H. & Xagoraraki, I. 2011 Removal of human enteric viruses by a full-scale membrane bioreactor during municipal wastewater processing. Water Res. 45, 2739-2750.
41. US Environmental Protection Agency 1999 Environmental regulations and technology: control of pathogens and vector attraction in sewage sludge. EPA/625/R-92-013. Office of Water, US Environmental Protection Agency, Washington, DC.
42. Veronica, A. 2008 Proper sanitization of sewage sludge: a critical issue of a sustainable society. Appl. Environ. Microbiol. 74, 5267-5275.
43. Vega, E., Lesikar, B. & Pillai, S. D. 2003 Transport and survival of bacterial and viral tracers through submerged-flow constructed wetland and sand-filter system. Bioresource Technol. 89, 49-56. (Pubitemid 36382917)
44. Vinje, J. 2008 Optimizing Molecular Methods to Detect Human Caliciviruses in Environmental Samples. US Environmental Protection Agency, Washington, DC.
45. Vinje, J. & Koopmans, M. P. 1996 Molecular detection and epidemiology of small round-structured viruses in outbreaks of gastroenteritis in the Netherlands. J. Infect. Dis. 174 (3), 610-615. (Pubitemid 26299697)
46. Waters, A., Coughlan, S., Dunford, L. & Hall, W. W. 2006 Molecular epidemiology of Norovirus strains circulating in Ireland from 2003 to 2004. Epidemiol. Infect. 134, 917-925. (Pubitemid 44336364)
47. WHO 1989 Health guidelines for the use of wastewater in agriculture and aquaculture. WHO Technical Report Series, No. 778. World Health Organizaion, Geneva, Switzerland.