Risk of norovirus gastroenteritis from consumption of vegetables irrigated with highly treated municipal wastewater-evaluation of methods to estimate sewage quality

Risk Analysis

Volumn 34, Issue 5, 2014, Pages 803-817

  Barker, S Fiona ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Quantitative microbial risk assessment (QMRA); Recycled water

Indexed keywords

ESTIMATION; HEALTH RISKS; RISK ASSESSMENT; RISK PERCEPTION; SEWAGE; VEGETABLES; WASTEWATER RECLAMATION; WASTEWATER TREATMENT;

DISABILITY ADJUSTED LIFE YEARS; EPIDEMIOLOGICAL METHODS; MELBOURNE , AUSTRALIA; MUNICIPAL WASTEWATERS; QUANTITATIVE MICROBIAL RISK ASSESSMENT; QUANTITATIVE MICROBIAL RISK ASSESSMENT (QMRA); RECYCLED WATER; TREATED EFFLUENT;

EFFLUENTS;

DISEASE PREVALENCE; EFFLUENT; EPIDEMIOLOGY; FOOD CONSUMPTION; GASTROENTERITIS; HEALTH RISK; IRRIGATION; MICROBIAL COMMUNITY; RECYCLING; RISK ASSESSMENT; RISK FACTOR; SENSITIVITY ANALYSIS; VEGETABLE; VIRUS; WASTEWATER;

AUSTRALIA; MELBOURNE; VICTORIA [AUSTRALIA];

NOROVIRUS;

SEWAGE; WASTE WATER;

AUSTRALIA; GASTROENTERITIS; HUMAN; IRRIGATION (AGRICULTURE); ISOLATION AND PURIFICATION; NOROVIRUS; RISK FACTOR; SEWAGE; VIROLOGY; WASTE WATER;

AGRICULTURAL IRRIGATION; GASTROENTERITIS; HUMANS; NOROVIRUS; QUEENSLAND; RISK FACTORS; SEWAGE; WASTE WATER;

EID: 84899547193     PISSN: 02724332     EISSN: 15396924     Source Type: Journal    
DOI: 10.1111/risa.12138     Document Type: Article

References (102)

1. Apostolidis N, Hertle C, Young R. Water recycling in Australia. Water, 2011; 3:869-881.
2. Boone SA, Gerba CP. Significance of fomites in the spread of respiratory and enteric viral disease. Applied and Environmental Microbiology, 2007; 73(6):1687-1696.
3. Matthews JE, Dickey BW, Miller RD, Felzer JR, Dawson BP, Lee AS, Rocks JJ, Kiel J, Montes JS, Moe CL, Eisenberg JNS, Leon JS. The epidemiology of published norovirus outbreaks: A review of risk factors associated with attack rate and genogroup. Epidemiology and Infection, 2012; 140 (7):1161-1172.
4. Ueki Y, Sano D, Watanabe T, Akiyama K, Omura T. Norovirus pathway in water environment estimated by genetic analysis of strains from patients of gastroenteritis, sewage, treated wastewater, river water and oysters. Water Research, 2005; 39(18):4271-4280.
5. Lodder WJ, De Roda Husman AM. Presence of noroviruses and other enteric viruses in sewage and surface waters in the Netherlands. Applied and Environmental Microbiology, 2005; 71(3):1453-1461.
6. Masago Y, Katayama H, Watanabe T, Haramoto E, Hashimoto A, Omura T, Hirata T, Ohgaki S. Quantitative risk assessment of noroviruses in drinking water based on qualitative data in Japan. Environmental Science and Technology, 2006; 40(23):7428-7433.
7. Ãstrom J, Petterson S, Bergstedt O, Pettersson TJR, Stenström TA. Evaluation of the microbial risk reduction due to selective closure of the raw water intake before drinking water treatment. Journal of Water and Health, 2007; 5(Supp. 1):81-97.
8. Viau EJ, Lee D, Boehm AB. Swimmer risk of gastrointestinal illness from exposure to tropical coastal waters impacted by terrestrial dry-weather runoff. Environmental Science and Technology, 2011; 45(17):7158-7165.
9. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, Tauxe RV. Food-related illness and death in the United States. Emerging Infectious Diseases, 1999; 5(5):607-625.
10. Esseili MA, Wang Q, Zhang Z, Saif LJ. Internalization of sapovirus, a surrogate for norovirus, in romaine lettuce and the effect of lettuce latex on virus infectivity. Applied and Environmental Microbiology, 2012; 78(17):6271-6279.
11. DiCaprio E, Ma Y, Purgianto A, Hughes J, Li J. Internalization and dissemination of human norovirus and animal caliciviruses in hydroponically grown romaine lettuce. Applied and Environmental Microbiology, 2012; 78(17):6143-6152.
12. van den Brandhof WE, de Wit GA, de Wit MAS, van Duynhoven YTHP. Costs of gastroenteritis in the Netherlands. Epidemiology and Infection, 2004; 132(2):211-221.
13. Gadiel D, Abelson P. The Economic Cost of Foodborne Disease in New Zealand. New Zealand Food Safety Authority, 2010.
14. Lopman BA, Reacher MH, Vipond IB, Hill D, Perry C, Halladay T, Brown DW, Edmunds WJ, Sarangi J. Epidemiology and cost of nosocomial gastroenteritis, Avon, England, 2002-2003. Emerging Infectious Diseases, 2004; 10(10):1827-1834.
15. McAuliffe C, Gregory D. Long term pathogen enumeration and removal across a 300 MLD wastewater treatment plant. In Water Reuse and Desalination: Water Scarcity Solutions for the 21st Century, 15-17 November 2010. Sydney, Australia, 2010.
16. Melbourne Water. Eastern Treatment Plant 2010. Available at: http://www.melbournewater.com.au/content/sewerage/eastern_treatment_plant/eastern_treatment_plant.asp, Accessed August 30, 2011.
17. Aitken D, Roder L, Everist P. Eastern Irrigation Scheme, Victoria: Operation of an ultra-filtration plant for a Class A recycled water scheme. Pp. 59-65 in 69th Annual Water Industry Engineers and Operators' Conference. Bendigo, Australia, 2006.
18. Melbourne Water. Sustainability Report: A Review of Melbourne Water's Performance in 2008/09. Melbourne, 2010.
19. TopAq. Eastern Irrigation Scheme 2010. Available at http://www.topaq.com.au, Accessed January 9, 2012.
20. NRMMC, EPHC, AHMC. Australian Guidelines for Water Recycling: Managing Health and Environmental Risks (Phase 1). Canberra: Natural Resource Management Ministerial Council, Environment Protection and Heritage Council, Australian Health Ministers' Conference, 2006.
21. EPAV. 1015 Guidelines for Environmental Management: Dual Pipe Water Recycling Schemes-Health and Environmental Risk Management. Southbank, Victoria: Environmental Protection Agency Victoria, 2005.
22. Barker SF, Faggian R, Hamilton AJ. A history of wastewater irrigation in Melbourne, Australia. Journal of Water Sustainability, 2012; 1(2):183-202.
23. Haramoto E, Katayama H, Oguma K, Yamashita H, Tajima A, Nakajima H, Ohgaki S. Seasonal profiles of human noroviruses and indicator bacteria in a wastewater treatment plant in Tokyo, Japan. Water Science and Technology, 2006; 54:301-308.
24. 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 Research, 2008; 42(6-7):1441-1448.
25. Ottoson J, Hansen A, Bjorlenius B, Norder H, Stenström TA. Removal of viruses, parasitic protozoa and microbial indicators in conventional and membrane processes in a wastewater pilot plant. Water Research, 2006; 40(7):1449-1457.
26. Ottoson J, Hansen A, Westrell T, Johansen K, Norder H, Stenström TA. Removal of noro- and enteroviruses, Giardia cysts, Cryptosporidium oocysts, and fecal indicators at four secondary wastewater treatment plants in Sweden. Water Environment Research, 2006; 78(8):828-834.
27. La Rosa G, Pourshaban M, Iaconelli M, Muscillo M. Quantitative real-time PCR of enteric viruses in influent and effluent samples from wastewater treatment plants in Italy. Annali dell'Istituto Superiore di Sanita, 2010; 46(3):266-273.
28. WHO. WHO Guidelines for the Safe Use of Wastewater, Excreta and Greywater. Volume II Wastewater Use in Agriculture. Geneva, Switzerland: World Health Organisation, 2006.
29. Soller J, Eisenberg JNS. An evaluation of parsimony for microbial risk assessment models. Environmetrics, 2008; 19:61-78.
30. Atmar RL. Noroviruses: State of the art. Food and Environmental Virology, 2010; 2(3):117-126.
31. Mattison K. Norovirus as a foodborne disease hazard. Advances in Food and Nutrition Research, 2011; 62(Supp):1-39.
32. Sinclair MI, Hellard ME, Wolfe R, Mitakakis TZ, Leder K, Fairley CK. Pathogens causing community gastroenteritis in Australia. Journal of Gastroenterology and Hepatology, 2005; 20(11):1685-1690.
33. USEPA. Exposure Factors Handbook: 2009 Update (EPA/600/R-09/052A). Washington, DC: Office of Research and Development, National Center for Environmental Assessment, U.S. Environmental Protection Agency, 2009.
34. Ausveg. Vegetable spotlight 2009. Available at http://ausveg.com.au/resources/statistics/vegetable-spotlight.htm, Accessed April 20, 2012.
35. ABS. 4306.0-Apparent Consumption of Foodstuffs, Australia, 1997-98 and 1998-99. Canberra: Australian Bureau of Statistics, Commonwealth of Australia, 2000.
36. DoHA. The 2007 National Children's Nutrition and Physical Activity Survey 2010. Available at: http://nesstar.assda.edu.au/webview/index.jsp?object=http://nesstar.assda.edu.au/obj/fStudy/au.edu.anu.assda.ddi.01132, Accessed November 19, 2011.
37. ABS. 4359.0 1995 How Australians Measure Up. Canberra: Australian Bureau of Statistics, 1998.
38. ABS. 3101.0-Australian Demographic Statistics, Mar 2011. Canberra: Australian Bureau of Statistics, 2011.
39. Hamilton AJ, Stagnitti F, Premier R, Boland AM, Hale G. Quantitative microbial risk assessment models for consumption of raw vegetables irrigated with reclaimed water. Applied and Environmental Microbiology, 2006; 72(5):3284-3290.
40. Shuval H, Lampert Y, Fattal B. Development of a risk assessment approach for evaluating wastewater reuse standards for agriculture. Water Science and Technology, 1997; 35:15-20.
41. Croci L, De Medici D, Scalfaro C, Fiore A, Toti L. The survival of hepatitis A virus in fresh produce. International Journal of Food Microbiology, 2002; 73(1):29-34.
42. Gulati BR, Allwood PB, Hedberg CW, Goyal SM. Efficacy of commonly used disinfectants for the inactivation of calicivirus on strawberry, lettuce, and a food-contact surface. Journal of Food Protection, 2001; 64(9):1430-1434.
43. Bae JY, Lee JS, Shin MH, Lee SH, Hwang IG. Effect of wash treatments on reducing human norovirus on iceberg lettuce and perilla leaf. Journal of Food Protection, 2011; 74(11):1908-1911.
44. Fraisse A, Temmam S, Deboosere N, Guillier L, Delobel A, Maris P, Vialette M, Morin T, Perelle S. Comparison of chlorine and peroxyacetic-based disinfectant to inactivate Feline calicivirus, Murine norovirus and Hepatitis A virus on lettuce. International Journal of Food Microbiology, 2011; 151(1):98-104.
45. Dawson DJ, Paish A, Staffell LM, Seymour IJ, Appleton H. Survival of viruses on fresh produce, using MS2 as a surrogate for norovirus. Journal of Applied Microbiology, 2005; 98(1):203-209.
46. Baert L, Uyttendaele M, Vermeersch M, Van Coillie E, Debevere J. Survival and transfer of murine norovirus 1, a surrogate for human noroviruses, during the production process of deep-frozen onions and spinach. Journal of Food Protection, 2008; 71(8):1590-1597.
47. Baert L, Vandekinderen I, Devlieghere F, Van EC, Debevere J, Uyttendaele M. Efficacy of sodium hypochlorite and peroxyacetic acid to reduce murine norovirus 1, B40-8, Listeria monocytogenes, and Escherichia coli 0157:H7 on shredded iceberg lettuce and in residual wash water. Journal of Food Protection, 2009; 72(5):1047-1054.
48. Butot S, Putallaz T, Sánchez G. Effects of sanitation, freezing and frozen storage on enteric viruses in berries and herbs. International Journal of Food Microbiology, 2008; 126(1-2):30-35.
49. Predmore A, Li J. Enhanced removal of a human norovirus surrogate from fresh vegetables and fruits by a combination of surfactants and sanitizers. Applied and Environmental Microbiology, 2011; 77(14):4829-4838.
50. Petterson SR, Ashbolt NJ, Sharma A. Microbial risks from wastewater irrigation of salad crops: A screening-level risk assessment. Water Environment Research, 2001; 73(6):667-672.
51. Petterson SR, Ashbolt NJ, Sharma A. Of: Microbial risks from wastewater irrigation of salad crops: A screening-level risk assessment. Water Environment Research, 2002; 74(4):411.
52. ABS. 3101.0-Australian Demographic Statistics, Mar 2012. Canberra: Australian Bureau of Statistics, 2012.
53. Hall G, Kirk M, Ashbolt R, Gregory J, Lalor K, Millard G, Raupach J, Sarna M, Stafford R. Results from the National Gastroenteritis Survey 2001-2002. Canberra, ACT: National Centre for Epidemiology & Population Health, Australian National University, 2004.
54. Hall G, Kirk M, Becker N, Gregory J, Unicomb L, Millard G, Stafford R, Lalor K. Estimating foodborne gastroenteritis, Australia. Emerging Infectious Diseases, 2005; 11(8):1257-1264.
55. Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, Graham DY. Norwalk virus shedding after experimental human infection. Emerging Infectious Diseases, 2008; 14(10):1553-1557.
56. Rao SSC. Oral rehydration for viral gastroenteritis in adults: A randomized, controlled trial of 3 solutions. JPEN, Journal of Parenteral and Enteral Nutrition, 2006; 30(5):433-439.
57. Melbourne Water. Essential facts: The sewerage system 2005. Available at: http://www.melbournewater.com.au/content/publications/publications.asp, Accessed May 25, 2007.
58. Melbourne Water. Western Treatment Plant Discharge Statistics. Melbourne: Melbourne Water, 2012.
59. Melbourne Water. Eastern Treatment Plant Upgrade: Information in Support of a Works Approval Application. Melbourne: Melbourne Water, 2009.
60. Barker SF, O'Toole J, Sinclair MI, Malawaraarachchi M, Leder K, Hamilton AJ. A probabilistic model of norovirus disease burden associated with greywater irrigation of home-produced lettuce in Melbourne, Australia. Water Research, 2013; 47:1421-1432.
61. Mitakakis TZ, Sinclair MI, Fairley CK, Lightbody PK, Leder K, Hellard ME. Food safety in family homes in Melbourne, Australia. Journal of Food Protection, 2004; 67(4):818-822.
62. Teunis PFM, Moe CL, Liu P, Miller SE, Lindesmith L, Baric RS, Le Pendu J, Calderon RL. Norwalk virus: How infectious is it? Journal of Medical Virology, 2008; 80(8):1468-1476.
63. Kemmeren JM, Mangen M-JJ, van Duynhoven YTHP, Havelaar AH. Priority Setting of Foodborne Pathogens: Disease Burden and Costs of Selected Enteric Pathogens (RIVM Report 330080001/2006). Bilthoven, The Netherlands: National Institute for Public Health and the Environment (RIVM), 2006.
64. Haagsma JA, Havelaar AH, Janssen BMF, Bonsel GJ. Disability adjusted life years and minimal disease: Application of a preference-based relevance criterion to rank enteric pathogens. Population Health Metrics, 2008; 6:1-8.
65. Cressey P, Lake R. Risk Ranking: DALY Estimates for Selected Foodborne Diseases in New Zealand Using Revised Dutch Disability Weights. Ilam, Christchurch: Institute of Environmental Science & Research Limited, 2009.
66. Lake RJ, Cressey PJ, Campbell DM, Oakley E. Risk ranking for foodborne microbial hazards in New Zealand: Burden of disease estimates. Risk Analysis, 2010; 30(5):743-752.
67. Soller JA, Bartrand T, Ashbolt NJ, Ravenscroft J, Wade TJ. Estimating the primary etiologic agents in recreational freshwaters impacted by human sources of faecal contamination. Water Research, 2010; 44(16):4736-4747.
68. Denborough MA, Downing HJ. Secretor status in asthma and hay fever. J Med Genet, 1968; 5:302-305.
69. Thorven M, Grahn A, Hedlund KO, Johansson H, Wahlfrid C, Larson G, Svensson L. A homozygous nonsense mutation (428G-A) in the human secretor (FUT2) gene provides resistance to symptomatic norovirus (GGII) infections. Journal of Virology, 2005; 79(24):15351-15355.
70. Sorensen G, Thompson B, Glanz K, Feng Z, Kinne S, DiClemente C, Emmons K, Heimendinger J, Probart C, Lichtenstein E. Work site-based cancer prevention: Primary results from the working well trial. American Journal of Public Health, 1996; 86(7):939-947.
71. Ma J, Betts NM, Horacek T, Georgiou C, White A. Assessing stages of change for fruit and vegetable intake in young adults: A combination of traditional staging algorithms and food-frequency questionnaires. Health Education Research, 2003; 18(2):224-236.
72. Willett W. Nutritional Epidemiology, 2nd ed. New York: Oxford University Press; 1998.
73. Walls HL, Wolfe R, Haby MM, Magliano DJ, De Courten M, Reid CM, McNeil JJ, Shaw J, Peeters A. Trends in BMI of urban Australian adults, 1980-2000. Public Health Nutrition, 2010; 13(5):631-638.
74. Penman AD, Johnson WD. The changing shape of the body mass index distribution curve in the population: Implications for public health policy to reduce the prevalence of adult obesity. Preventing Chronic Disease, 2006; 3(3):1-4.
75. Fatica MK, Schneider KR. The use of chlorination and alternative sanitizers in the produce industry. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources, 2009; 4(9):1-10.
76. Gil MI, Selma MV, López-Gálvez F, Allende A. Fresh-cut product sanitation and wash water disinfection: Problems and solutions. International Journal of Food Microbiology, 2009; 134(1-2):37-45.
77. Allwood PB, Malik YS, Hedberg CW, Goyal SM. Effect of temperature and sanitizers on the survival of feline calicivirus, Escherichia coli, and F-specific coliphage MS2 on leafy salad vegetables. Journal of Food Protection, 2004; 67(7):1451-1456.
78. WHO. WHO Guidelines for the Safe Use of Wastewater, Excreta and Greywater. Geneva, Switzerland: World Health Organisation, 2006.
79. Ayuso-Gabella N, Page D, Masciopinto C, Aharoni A, Salgot M, Wintgens T. Quantifying the effect of managed aquifer recharge on the microbiological human health risks of irrigating crops with recycled water. Agricultural Water Management, 2011; 99(1):93-102.
80. Mara D, Sleigh A. Estimation of norovirus infection risks to consumers of wastewater-irrigated food crops eaten raw. Journal of Water and Health, 2010; 8(1):39-43.
81. Seidu R, Heistad A, Amoah P, Drechsel P, Jenssen PD, Stenström TA. Quantification of the health risk associated with wastewater reuse in Accra, Ghana: A contribution toward local guidelines. Journal of Water and Health, 2008; 6(4):461-471.
82. Flint JA, Van Duynhoven YT, Angulo FJ, DeLong SM, Braun P, Kirk M, Scallan E, Fitzgerald M, Adak GK, Sockett P, Ellis A, Hall G, Gargouri N, Walke H, Braam P. Estimating the burden of acute gastroenteritis, foodborne disease, and pathogens commonly transmitted by food: An international review. Clinical Infectious Diseases, 2005; 41(5):698-704.
83. Wheeler JG, Sethi D, Cowden JM, Wall PG, Rodrigues LC, Tompkins DS, Hudson MJ, Roderick PJ. Study of infectious intestinal disease in England: Rates in the community, presenting to general practice, and reported to national surveillance. British Medical Journal, 1999; 318(7190):1046-1050.
84. Carter MJ. Enterically infecting viruses: Pathogenicity, transmission and significance for food and waterborne infection. Journal of Applied Microbiology, 2005; 98(6):1354-1380.
85. de Wit MAS, Koopmans MPG, Kortbeek LM, Wannet WJB, Vinje J, van Leusden F, Bartelds AIM, van Duynhoven YTHP. Sensor, a population-based cohort study on gastroenteritis in the Netherlands: Incidence and etiology. American Journal of Epidemiology, 2001; 154(7):666-674.
86. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerging Infectious Diseases, 2008; 14(8):1224-1231.
87. EPAV. 464.2 Guidelines for environmental management: Use of reclaimed water [guideline online: Environmental Protection Agency Victoria], 2003. Available at: http://epanote2.epa.vic.gov.au/EPA/Publications.nsf/PubDocsLU/464.2?OpenDocument, Accessed June 30, 2008.
88. Pintar KDM, Fazil A, Pollari F, Waltner-Toews D, Charron DF, McEwen SA, Walton T. Considering the risk of infection by Cryptosporidium via consumption of municipally treated drinking water from a surface water source in a southwestern Ontario community. Risk Analysis, 2012; 32(7):1122-1238.
89. Teunis PFM, Nagelkerke NJD, Haas CN. Dose response models for infectious gastroenteritis. Risk Analysis, 1999; 19(6):1251-1260.
90. Chevrefils G, Caron E, Wright H, Sakamoto G, Payment P, Barbeau B, Cairns B. UV dose required to achieve incremental log inactivation of bacteria, protozoa and viruses. IUVA News, 2006; 8(1):38-45.
91. DH. Guidelines for Validating Treatment Processes for Pathogen Reduction. Supporting Class A Recycled Water Schemes in Victoria. Victoria: Department of Health, 2013.
92. Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, Lindblad L, Stewart P, Lependu J, Baric R. Human susceptibility and resistance to Norwalk virus infection. Nature Medicine, 2003; 9(5):548-553.
93. Johnson PC, Mathewson JJ, DuPont HL, Greenberg HB. Multiple-challenge study of host susceptibility to Norwalk gastroenteritis in US adults. Journal of Infectious Diseases, 1990; 161(1):18-21.
94. Le Pendu J, Ruvoen-Clouet N, Kindberg E, Svensson L. Mendelian resistance to human norovirus infections. Seminars in Immunology, 2006; 18(6):375-386.
95. Signor RS, Ashbolt NJ. Comparing probabilistic microbial risk assessments for drinking water against daily rather than annualised infection probability targets. Journal of Water and Health, 2009; 7(4):535-543.
96. Buckland ST. Monte Carlo confidence intervals. Biometrics, 1984; 40:811-817.
97. Xue J, Zartarian VG, Özkaynak H, Dang W, Glen G, Smith L, Stallings C. A probabilistic arsenic exposure assessment for children who contact chromated copper arsenate (CCA)-treated playsets and decks, part 2: Sensitivity and uncertainty analyses. Risk Analysis, 2006; 26(2):533-541.
98. Julian TR, Canales RA, Leckie JO, Boehm AB. A model of exposure to rotavirus from nondietary ingestion iterated by simulated intermittent contacts. Risk Analysis, 2009; 29(5):617-632.
99. Enger KS, Nelson KL, Clasen T, Rose JB, Eisenberg JNS. Linking quantitative microbial risk assessment and epidemiological data: Informing safe drinking water trials in developing countries. Environmental Science & Technology, 2012; 46(9):5160-5167.
100. Ferrer A, Nguyen-Viet H, Zinsstag J. Quantification of diarrhea risk related to wastewater contact in Thailand. EcoHealth, 2012; 9(1):49-59.
101. The R Foundation for Statistical Computing. R Project for Statistical Computing, 2011. Available at: http://www.r-project.org/, Accessed September 1, 2011.
102. Barker SF, Packer M, Scales P, Gray S, Snape I, Hamilton AJ. Direct potable reuse in small, remote communities: Required pathogen reductions for reuse at Davis, Antarctica. Science of the Total Environment, 2013; 461 The 462:723 The 733.