A case study of enteric virus removal and insights into the associated risk of water reuse for two wastewater treatment pond systems in Bolivia

Water Research

Volumn 65, Issue , 2014, Pages 257-270

  Symonds, E M ^a   Verbyla, M E ^b   Lukasik, J O ^c   Kafle, R C ^d,e   Breitbart, M ^a   Mihelcic, J R ^b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b University of South Florida   (United States)

^c Biological Consulting Services of North Florida   (United States)

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

^e SAM HOUSTON STATE UNIVERSITY   (United States)

Author keywords

Norovirus; Pepper mild mottle virus; Rotavirus; Sanitation; Stabilization pond; Upflow anaerobic sludge blanket reactor

Indexed keywords

CELL CULTURE; EFFLUENTS; HEALTH RISKS; POLYMERASE CHAIN REACTION; PONDING; RISK ASSESSMENT; SANITATION; STABILIZATION PONDS; VIRUSES; WASTEWATER RECLAMATION; WASTEWATER TREATMENT; WATER CONSERVATION;

DISABILITY ADJUSTED LIFE YEARS; NOROVIRUS; PEPPER MILD MOTTLE VIRUS; QUANTITATIVE MICROBIAL RISK ASSESSMENT; QUANTITATIVE POLYMERASE CHAIN REACTION; ROTAVIRUSES; UP-FLOW ANAEROBIC SLUDGE BLANKET REACTORS; WASTE-WATER TREATMENT PONDS;

LAKES;

VIRUS VACCINE; WASTE WATER;

CONCENTRATION (COMPOSITION); MATURATION; MICROBIAL ECOLOGY; POLYMERASE CHAIN REACTION; VIRUS; WASTEWATER; WATER QUALITY; WATER TREATMENT; WATER USE;

ADULT; AGRICULTURAL WORKER; ARTICLE; BOLIVIA; BULK DENSITY; CHILD; CONTROLLED STUDY; CULTURE TECHNIQUE; CYTOPATHOGENIC EFFECT; DISABILITY; DISABILITY ADJUSTED LIFE YEAR; DOSE RESPONSE; EFFLUENT; ENTERIC VIRUS; ENTEROVIRUS; EQUINE VIRAL ARTERITIS VIRUS; GENETIC RESISTANCE; HUMAN; LIMIT OF DETECTION; LIMIT OF QUANTITATION; MOST PROBABLE NUMBER; NONHUMAN; NOROVIRUS; NOROVIRUS GENOTYPE 1; PEPPER MILD MOTTLE VIRUS; PLANT VIRUS; POLYMERASE CHAIN REACTION; POND; PRIORITY JOURNAL; QUALITY ADJUSTED LIFE YEAR; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RISK ASSESSMENT; RNA PURIFICATION; ROTAVIRUS; UPFLOW REACTOR; VIRAL CONTAMINATION; VIRUS CONCENTRATION; VIRUS ISOLATION; VIRUS PARTICLE; VIRUS PURIFICATION; WASTE COMPONENT REMOVAL; WASTE WATER MANAGEMENT; WASTE WATER RECYCLING; WORLD HEALTH ORGANIZATION; ANIMAL; CELL LINE; CHLOROCEBUS AETHIOPS; GENETICS; IRRIGATION (AGRICULTURE); ISOLATION AND PURIFICATION; PARTICLE SIZE; PROCEDURES; SEWAGE; VIROLOGY; WASTE WATER; WATER MANAGEMENT; WATER SUPPLY;

BOLIVIA;

AGRICULTURAL IRRIGATION; ANIMALS; BOLIVIA; CELL LINE; CERCOPITHECUS AETHIOPS; ENTEROVIRUS; PARTICLE SIZE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RISK ASSESSMENT; WASTE DISPOSAL, FLUID; WASTE WATER; WATER PURIFICATION; WATER SUPPLY;

EID: 84906097249     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2014.07.032     Document Type: Article

References (66)

1. Baum R., Luh J., Bartram J. Sanitation: a global estimate of sewerage connections without treatment and the resulting impact on MDG progress. Environ. Sci. Technol. 2013, 47(4):1994-2000.
2. Bausum H.T., Schaub S.A., Rose W.E., Gibbs P.H. Enteric Virus Removal in Wastewater Treatment Lagoon Systems 1983, Publication No. EPA-600/51-83-012, U.S. Environmental Protection Agency, Research Triangle Park, NC, USA.
3. Barker S.F., Packer M., Scales P.J., Gray S., Snape I., Hamilton A.J. Pathogen reduction requirements for direct potable reuse in Antarctica: evaluating human health risks in small communities. Sci. Total Environ. 2013, 461-462:723-733.
4. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55(4):611-622.
5. Cliver D.O. Experimental infection by waterborne enteroviruses. J. Food Prot. 1981, 44:861-865.
6. Cornejo P.K., Zhang Q., Mihelcic J.R. Quantifying benefits of resource recovery from sanitation provision in a developing world setting. J. Environ. Manag. 2013, 131:7-15.
7. Da Silva A.K., Le Guyader F.S., Le Saux J.C., Pommepuy M., Montgomery M.A., Elimelech M. Norovirus removal and particle association in a waste stabilization pond. Environ. Sci. Technol. 2008, 42(24):9151-9157.
8. de Lemos Chernicharo C.A. Anaerobic Reactors. Biological Wastewater Treatment Series 2007, vol. 4. IWA Publishing, London, UK.
9. Drechsel P., Raschid-Sally L., Williams S., Weale J. Recycling Realities: Managing Health Risks to Make Wastewater an Asset 2006, Water Policy Briefing, International Water Management Institute, Colombo, Sri Lanka.
10. El-Deeb Ghazy M.M., El-Senousy W.M., Abdel-Aatty A.M., Kamel M. Performance evaluation of a waste stabilization pond in a rural area in Egypt. Am. J. Environ. Sci. 2008, 4(4):316-325.
11. Feachem R.G., Bradley D.J., Garelick H., Mara D.D. Sanitation and Disease: Health Aspects of Excreta and Wastewater Management 1983, John Wiley & Sons, Chichester, England.
12. Fry L.M., Mihelcic J.R., Watkins D.W. Water and nonwater-related challenges of achieving global sanitation coverage. Environ. Sci. Technol. 2008, 42(12):4298-4304.
13. Fry L.M., Watkins D.W., Reents N., Rowe M.D., Mihelcic J.R. Climate change and development impacts on the sustainability of spring-fed water supply systems in the Alto Beni region of Bolivia. J. Hydrol. 2012, 468:120-129.
14. Fuchs V.J., Mihelcic J.R. Analysing appropriateness in sanitation projects in the Alto Beni region of Bolivia. Waterlines 2011, 30(2):122-134.
15. Haramoto E., Katayama H., Ohgaki S. Quantification and genotyping of Torque Teno Virus at a wastewater treatment plant in Japan. Appl. Environ. Microbiol. 2008, 74(23):7434-7436.
16. Havelaar A.H., Melse J.M. Quantifying Public Health Risk in the WHO Guidelines for Drinking-water Quality: a Burden of Disease Approach 2003, RIVM report 734301022, Rijksinstituut voor Volksgezondheid en Milieu (RIVM), Bilthoven, The Netherlands.
17. Howard G., Ahmed M.F., Mahumd S.G., Teunis P.F.M., Davison A., Deere D. Disease burden estimation to support policy decision-making and research prioritization for arsenic mitigation. J. Water Health 2007, 5(1):67-81.
18. Huang Y. Enteroviruses Dose Response Models 2013, Quantitative Microbial Risk Assessment Wiki. Center for Advancing Microbial Risk Assessment, Michigan State University, (accessed 07.02.14.). http://qmrawiki.msu.edu/index.php?title=Enteroviruses%253A_Dose_Response_Models.
19. Keraita B., Drechsel P., Klutse A., Cofie O.O. On-farm Treatment Options for Wastewater, Freywater and Fecal Sludge with Special Reference to West Africa 2014, CGIAR Research Program on Water, Land and Ecosystems (Resource Recovery and Reuse Series 1). International Water Management Institute, Colombo, Sri Lanka.
20. Kitajima M., Iker B.C., Pepper I.L., Gerba C.P. Relative abundance and treatment reduction of viruses during wastewater treatment processes - identification of potential viral indicators. Sci. Total Environ. 2014, 488-489(0):290-296.
21. Kohn T., Nelson K.L. Sunlight-mediated inactivation of MS2 coliphage via exogenous singlet oxygen produced by sensitizers in natural waters. Environ. Sci. Technol. 2006, 41(1):192-197.
22. Lettinga G. The route of anaerobic waste (water) treatment toward global acceptance. Environmental Anaerobic Technology- Applications and New Developments 2010, 1-15. Imperial College Press, London, U.K. H.H.P. Fang (Ed.).
23. Limsawat S., Ohgaki S. Fate of liberated viral RNA in wastewater determined by PCR. Appl. Environ. Microbiol. 1997, 63(7):2932-2933.
24. Liu Y.Q., Liu Y., Tay J.H. The effects of extracellular polymeric substances on the formation and stability of biogranules. Appl. Microbiol. Biotechnol. 2004, 65(2):143-148.
25. Mara D.D., Sleigh P.A., Blumenthal U.J., Carr R.M. Health risks in wastewater irrigation: comparing estimates from quantitative microbial risk analyses and epidemiological studies. J. Water Health 2007, 5(1):39-50.
26. Mara D.D., Hamilton A.J., Sleigh A., Karavarsamis N. Discussion Paper: Options for Updating the 2006 WHO Guidelines 2010, WHO-FAO-IDRC-IWMI.
27. Maynard H.E., Ouki S.K., Williams S.C. Tertiary lagoons: a review of removal mechanisms and performance. Water Res. 1999, 33(1):1-13.
28. McBride G.B., Stott R., Miller W., Bambic D., Wuertz S. Discharge-based QMRA for estimation of public health risks from exposure to stormwater-borne pathogens in recreational waters in the United States. Water Res. 2013, 47(14):5282-5297.
29. McCarty P.L., Bae J., Kim J. Domestic wastewater treatment as a net energy producer-can this be achieved?. Environ. Sci. Technol. 2011, 45(17):7100-7106.
30. Mok H.F., Hamilton A.J. Exposure factors for wastewater-irrigated asian vegetables and a probabilistic rotavirus disease burden model for their consumption. Risk Anal. 2014, 34(4):602-613.
31. Mok H.F., Barker S.F., Hamilton A.J. A probabilistic quantitative microbial risk assessment model of norovirus disease burden from wastewater irrigation of vegetables in Shepparton, Australia. Water Res. 2014, 54:347-362.
32. Muga H.E., Mihelcic J.R., Reents N.W., Morales S., Gemio G., Ballard M., Fuchs V.J., Hanson C.M., Johnson E.M., Hoyt A.M. Treatment performance of wastewater lagoons in South Yungas province of Bolivia. Procedings of the World Environmental and Water Resource Congress 2009, ASCE, Kansas City, MO.
33. Oakley S.M. The need for wastewater treatment in Latin America: a case study of the use of wastewater stabilization ponds in Honduras. Small Flows Q. 2005, 6(2):36-51.
34. Oragui J.I., Curtis T.P., Silva S.A., Mara D.D. The removal of excreted bacteria and viruses in deep waste stabilization ponds in northeast Brazil. Water Sci. Technol. 1987, 19(3-4):569-573.
35. Oragui J.I., Arridge H., Mara D.D., Pearson H.W., Silva S.A. Rotavirus removal in experimental waste stabilization pond systems with different geometries and configurations. Water Sci. Technol. 1995, 31(12):285-290.
36. O'Ryan M.L., Peña A., Vergara R., Díaz J., Mamani N., Cortés H., Lucero Y., Vidal R., Osorio G., Santolaya M.E., Hermosilla G., Prado V.J. Prospective characterization of norovirus compared with rotavirus acute diarrhea episodes in chilean children. Pediatric Infect. Dis. J. 2010, 29(9):855-859.
37. Ottoson J., Stenström T.A. Faecal contamination of greywater and associated microbial risks. Water Res. 2003, 37(3):645-655.
38. Patel M.M., Patzi M., Pastor D., Nina A., Roca Y., Alvarez L., Iniguez V., Rivera R., Tam K.I., Quaye O., Bowen M., Parashar U., De Oliveira L.H. Effectiveness of monovalent rotavirus vaccine in Bolivia: case-control study. BMJ: Br. Med. J. 2013, 346:f3726.
39. Prüss-Üstün A., Bos R., Gore F., Bartram J. Safer Water, Better Health: Costs, Benefits and Sustainability of Interventions to Protect and Promote Health 2008, World Health Organization, Geneva, Switzerland.
40. Raschid-Sally L., Jayakody P. Drivers and Characteristics of Wastewater Agriculture in Developing Countries: Results from a Global Assessment 2008, IWMI Report 127, International Water Management Institute, Colombo, Sri Lanka.
41. Rao V.C., Lakhe S.B., Waghmare S.V. Virus removal in waste stabilization ponds in India. Water Res. 1981, 15(7):773-778.
42. Rodríguez R.A., Gundy P.M., Gerba C.P. Comparison of BGM and PLC/PRC/5 cell lines for total culturable viral assay of treated sewage. Appl. Environ. Microbiol. 2008, 74(9):2583-2587.
43. Romero C., Mamani N., Halvorsen K., Iñiguez V. Enfermedades diarreicas agudas asociadas a rotavirus. (Acute diarrheal diseases associated with rotavirus). Revista Chilena de Pediatría 2007, 78(5):549-558.
44. Rosario K., Symonds E.M., Sinigalliano C., Stewart J., Breitbart M. Pepper Mild Mottle Virus as an indicator of fecal pollution. Appl. Environ. Microbiol. 2009, 75(22):7261-7267.
45. Schijven J., de Roda Husman A.M. A survey of diving behavior and accidental water ingestion among Dutch occupational and sport divers to assess the risk of infection with waterborne pathogenic microorganisms. Environ. Health Perspect. 2006, 114(5):712-717.
46. Seidu R., Heistad A., Amoah P., Drechsel P., Jenssen P.D., Stenström T.A. Quantification of the health risk associated with wastewater reuse in Accra, Ghana: a contribution toward local guidelines. J. Water Health 2008, 6(4):461-471.
47. Shuval H.I.) Wastewater Irrigation in Developing Countries: Health Effects and Technical Solutions 1990, Summary of World Bank Technical Paper 51. Integrated Resource Recovery Project (GLO/84/007), Washington, D.C.
48. Silverman A.I., Akrong M.O., Drechsel P., Nelson K.L. On-farm treatment of wastewater used for vegetable irrigation: bacteria and virus removal in small ponds in Accra, Ghana. J. Water Reuse Desalin. 2014, (in press).
49. Sivaganesan M., Haugland R.A., Chern E.C., Shanks O.C. Improved strategies and optimization of calibration models for real-time PCR absolute quantification. Water Res. 2010, 44(16):4726-4735.
50. Svraka S., van der Veer B., Duizer E., Dekkers J., Koopmans M., Vennema H. Novel approach for detection of enteric viruses to enable syndrome surveillance of acute viral gastroenteritis. J. Clin. Microbiol. 2009, 47(6):1674-1679.
51. Tanaka H., Asano T., Schroeder E.D., Tchobanoglous G. Estimating the safety of wastewater reclamation and reuse using enteric virus monitoring data. Water Environ. Res. 1998, 70(1):39-51.
52. Templeton M.R., Andrews R.C., Hofmann R. Particle-associated viruses in water: impacts on disinfection processes. Crit. Rev. Environ. Sci. Technol. 2008, 38(3):137-164.
53. Teunis P.F.M., Havelaar A.H. The Beta Poisson dose-response model is not a single-hit model. Risk Anal. 2000, 20(4):513-520.
54. Teunis P.F.M., Moe C.L., Liu P., Miller S.E., Lindesmith L., Baric R.S., Le Pendu J., Calderon R.L. Norwalk virus: how infectious is it?. J. Med. Virol. 2008, 80:1468-1476.
55. U.S.Environmental Protection Agency USEPA Manual of Methods for Virology 2001, Publication No. EPA/600/4-84/013 (N14), Office of Research and Development, Washington, D.C., USA.
56. U.S.Environmental Protection Agency Environmental Regulations and Technology: Control of Pathogens and Vector Attraction in Sewage Sludge (Appendix H) 2003, Publication No. EPA/625/R-92/013, Office of Research and Development, Washington, D.C., USA.
57. U.S.Environmental Protection Agency Method 1615:Measurement of Enterovirus and Norovirus Occurrence in Water by Culture and RT-qPCR 2012, Publication No. EPA/600/R-10/181, Office of Research and Development, Washington, D.C., USA.
58. Verbyla M.E., Oakley S.M., Mihelcic J.R. Wastewater infrastructure for small cities in an urbanizing world: integrating protection of human health and the environment with resource recovery and food security. Environ. Sci. Technol. 2013, 47(8):3598-3605.
59. Verbyla M.E., Oakley S.M., Lizima L.A., Zhang J., Iriarte M., Tejada-Martinez A.E., Mihelcic J.R. Taenia eggs in a stabilization pond system with poor hydraulics: concern for human cysticercosis?. Water Sci. Technol. 2013, 68(12):2698-2703.
60. Viceministerio de Recursos Hídricos y Riego Agenda del Riego 2025 (Irrigation Agenda for 2025) 2013, La Paz, Bolivia, (accessed 07.02.14.). http://www.proagro-bolivia.org/files/Agenda_de_Riego_2025.pdf.
61. Von Sperling M. Modelling of coliform removal in 186 facultative and maturation ponds around the world. Water Res. 2005, 39(20):5261-5273.
62. Von Sperling M., Mascarenhas L.C.A.M. Performance of very shallow ponds treating effluents from UASB reactors. Water Sci. Technol. 2005, 51(12):83-90.
63. Von Sperling M., Bastos R.K.X., Kato M.T. Removal of E. coli and helminth eggs in UASB: polishing pond systems in Brazil. Water Sci. Technol. 2005, 51(12):91-97.
64. Ward R.L., Bernstein D.I., Young E.C., Sherwood J.R., Knowlton D.R., Schiff G.M. Human rotavirus studies in volunteers: determination of infectious dose and serological response to infection. Journal of Infectious Diseases 1986, 154(5):871-880.
65. World Health Organization Guidelines for the Safe Use of Wastewater, Excreta and Greywater: Volume II Wastewater Use in Agriculture 2006, WHO Press, Geneva, Switzerland.
66. World Health Organization Immunization, Vaccines and Biologicals: Data, Statistics and Graphics 2014, WHO/UNICEF Joint Reporting Form, (accessed 07.02.14.). http://apps.who.int/immunization_monitoring/globalsummary/timeseries/tscoveragerota_last.html.