Abstract
Typical recreational water risk to swimmers is assessed using epidemiologically derived correlations by means of fecal indicator bacteria (FIB). It has been documented that concentrations of FIB do not necessarily correlate well with protozoa and viral pathogens, which pose an actual threat of illness and thus sometimes may not adequately assess the overall microbial risks from water resources. Many of the known pathogens have dose-response relationships; however, measuring water quality for all possible pathogens is impossible. In consideration of a typical freshwater receiving secondarily treated effluent, we investigated the level of consistency between the indicator-derived correlations and the sum of risks from six reference pathogens using a quantitative microbial risk assessment (QMRA) approach. Enterococci and E. coli were selected as the benchmark FIBs, and norovirus, human adenovirus (HAdV), Campylobacter jejuni, Salmonella enterica, Cryptosporidium spp., and Giardia spp. were selected as the reference pathogens. Microbial decay rates in freshwater and uncertainties in exposure relationships were considered in developing our analysis. Based on our exploratory assessment, the total risk was found within the range of risk estimated by the indicator organisms, with viral pathogens as dominant risk agents, followed by protozoan and bacterial pathogens. The risk evaluated in this study captured the likelihood of gastrointestinal illnesses only, and did not address the overall health risk potential of recreational waters with respect to other disease endpoints. Since other highly infectious pathogens like hepatitis A and Legionella spp. were not included in our analysis, these estimates should be interpreted with caution.
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References
Ahmed W, Gyawali P, Sidhu J, Toze S (2014) Relative inactivation of faecal indicator bacteria and sewage markers in freshwater and seawater microcosms. Lett Appl Microbiol 59:348–354
Ahmed W, Harwood V, Gyawali P, Sidhu J, Toze S (2015) Comparison of concentration methods for quantitative detection of sewage-associated viral markers in environmental waters. Appl Environ Microbiol 81:2042–2049
Anderson KL, Whitlock JE, Harwood VJ (2005) Persistence and differential survival of fecal indicator bacteria in subtropical waters and sediments. Appl Environ Microbiol 71:3041–3048
Ashbolt NJ (2015) Microbial contamination of drinking water and human health from community water systems. Current Environ Health Reports 2:95–106. https://doi.org/10.1007/s40572-014-0037-5
Ashbolt NJ, Schoen ME, Soller JA, Roser DJ (2010) Predicting pathogen risks to aid beach management: the real value of quantitative microbial risk assessment (QMRA). Water Res 44:4692–4703
Bae J, Schwab KJ (2008) Evaluation of murine norovirus, feline calicivirus, poliovirus, and MS2 as surrogates for human norovirus in a model of viral persistence in surface water and groundwater. Appl Environ Microbiol 74:477–484
Bae S, Wuertz S (2012) Survival of host-associated bacteroidales cells and their relationship with enterococcus spp., campylobacter jejuni, salmonella enterica serovar typhimurium, and adenovirus in freshwater microcosms as measured by propidium monoazide-quantitative PCR. Appl Environ Microbiol 78:922–932
Betancourt WQ, Gerba CP (2016) Rethinking the significance of Reovirus in water and wastewater. Food Environ Virology 8:161–173
Brookes JD, Antenucci J, Hipsey M, Burch MD, Ashbolt NJ, Ferguson C (2004) Fate and transport of pathogens in lakes and reservoirs. Environ Int 30:741–759
Cabelli VJ (1989) Swimming-associated illness and recreational water quality criteria. Water Sci Technol 21:13–21
Cacciò SM, De Giacomo M, Aulicino FA, Pozio E (2003) Giardia cysts in wastewater treatment plants in Italy. Appl Environ Microbiol 69:3393–3398
Castro-Hermida JA, García-Presedo I, Almeida A, González-Warleta M, Da Costa JMC, Mezo M (2008) Contribution of treated wastewater to the contamination of recreational river areas with cryptosporidium spp. and giardia duodenalis. Water Res 42:3528–3538
Chaudhry RM, Nelson KL, Drewes JE (2015) Mechanisms of pathogenic virus removal in a full-scale membrane bioreactor. Environ Sci Technol 49:2815–2822
Chaudhry RM, Hamilton KA, Haas CN, Nelson KL (2017) Drivers of microbial risk for direct potable reuse and de facto reuse treatment schemes: the impacts of source water quality and blending. Int J Environ Res Public Health 14:635
Chauret C, Nolan K, Chen P, Springthorpe S, Sattar S (1998) Aging of Cryptosporidium parvum oocysts in river water and their susceptibility to disinfection by chlorine and monochloramine. Can J Microbiol 44:1154–1160
Chauret C, Springthorpe S, Sattar S (1999) Fate of cryptosporidium oocysts, giardia cysts, and microbial indicators during wastewater treatment and anaerobic sludge digestion. Can J Microbiol 45:257–262
Cole L, Schupp D, Erlandsen S (1989) Viability of giardia cysts suspended in lake, river, and tap water. Appl Environ Microbiol 55:1223–1229
Coleman ME, Marks HM (2000) Mechanistic modeling of salmonellosis. Quant Microbiol 2:227–247
Couch RB, Cate TR, Douglas Jr RG, Gerone PJ, Knight V (1966a) Effect of route of inoculation on experimental respiratory viral disease in volunteers and evidence for airborne transmission. Bacteriol Rev 30:517
Couch RB, Cate TR, Fleet WF, Gerone PJ, Knight V (1966b) Aerosol-induced adenoviral illness resembling the naturally occurring illness in military recruits. Am Rev Respir Dis 93:529–535
Couch R, Knight V, Douglas Jr R, Black S, Hamory B (1969) The minimal infectious dose of adenovirus type 4; the case for natural transmission by viral aerosol. Trans Am Clin Climatol Assoc 80:205
Couch R, Douglas Jr R, Lindgren K, Gerone P, Knight V (1970) Airborne transmission of respiratory infection with coxsackievirus a type 21. Am J Epidemiol 91:78–86
Dietrich JP, Darby JL, Loge FJ (2009) Potential health risks associated with particles in reclaimed wastewater. J Environ Eng 135:285–290
Dufour A, Ballentine R (1986) Ambient water quality criteria for bacteria, 1986: bacteriological ambient water quality criteria for marine and fresh recreational waters. National Technical Information Service, Department of Commerce, US,
Dufour AP, Evans O, Behymer TD, Cantu R (2006) Water ingestion during swimming activities in a pool: a pilot study. J Water Health 4:425–430
DuPont HL, Chappell CL, Sterling CR, Okhuysen PC, Rose JB, Jakubowski W (1995) The infectivity of Cryptosporidium parvum in healthy volunteers. N Engl J Med 332:855–859
Easton J, Lalor M, Gauthier JJ, Pitt R in-situ die-off of indicator bacteria and pathogens. In: Proceedings: AWRA’s 1999 annual water resources conference-watershed management to protect declining species, 1999
Eftim SE, Hong T, Soller J, Boehm A, Warren I, Ichida A, Nappier SP (2017) Occurrence of norovirus in raw sewage–a systematic literature review and meta-analysis. Water Res 111:366–374
Eisenberg JN, Seto EY, Olivieri AW, Spear RC (1996) Quantifying water pathogen risk in an epidemiological framework. Risk Anal 16:549–563
Gómez M, Plaza F, Garralón G, Pérez J, Gómez MA (2007) A comparative study of tertiary wastewater treatment by physico-chemical-UV process and macrofiltration–ultrafiltration technologies. Desalination 202:369–376
Haas CN (1983) Effect of effluent disinfection on risks of viral disease transmission via recreational water exposure. Journal (Water Pollution Control Federation) 55:1111–1116
Haas C (2012) Quantitative Microbial Risk Assessment (QMRA) Wiki
Haas CN, Rose JB, Gerba C, Regli S (1993) Risk assessment of virus in drinking water. Risk Anal 13:545–552
Haas CN, Crockett CS, Rose JB, Gerba CP, Fazil AM (1996) Assessing the risk posed by oocysts in drinking water. Am Water Works Assoc J 88:131–136
Haas CN, Rose JB, Gerba CP (1999) Quantitative microbial risk assessment. John Wiley & Sons,
Haas CN, Rose JB, Gerba CP (2014) Risk Assessment Paradigms. In: Quantitative microbial risk assessment. John Wiley & Sons, Inc, pp 63–89. doi:https://doi.org/10.1002/9781118910030.ch3
Harwood VJ, Levine AD, Scott TM, Chivukula V, Lukasik J, Farrah SR, Rose JB (2005) Validity of the indicator organism paradigm for pathogen reduction in reclaimed water and public health protection. Appl Environ Microbiol 71:3163–3170
He J-W, Jiang S (2005) Quantification of enterococci and human adenoviruses in environmental samples by real-time PCR. Appl Environ Microbiol 71:2250–2255
Heerden J, Ehlers M, Vivier J, Grabow W (2005) Risk assessment of adenoviruses detected in treated drinking water and recreational water. J Appl Microbiol 99:926–933
Hewitt J, Leonard M, Greening GE, Lewis GD (2011) Influence of wastewater treatment process and the population size on human virus profiles in wastewater. Water Res 45:6267–6276
Hlavsa MC et al (2011) Surveillance for waterborne disease outbreaks and other health events associated with recreational water—United States, 2007–2008. MMWR Surveill Summ 60:1–32
Hurst CJ, McClellan KA, Benton WH (1988) Comparison of cytopathogenicity, immunofluorescence and in situ DNA hybridization as methods for the detection of adenoviruses. Water Res 22:1547–1552
Jacangelo JG, Trussell RR (2002) International report: water and wastewater disinfection-trends, issues and practices water science and technology. Water Supply 2:147–157
Kauppinen A, Miettinen IT (2017) Persistence of norovirus GII genome in drinking water and wastewater at different temperatures. Pathogens 6:48
Kay D, Stapleton CM, Wyer MD, McDonald AT, Crowther J, Paul N, Jones K, Francis C, Watkins J, Wilkinson J, Humphrey N, Lin B, Yang L, Falconer RA, Gardner S (2005) Decay of intestinal enterococci concentrations in high-energy estuarine and coastal waters: towards real-time T 90 values for modelling faecal indicators in recreational waters. Water Res 39:655–667
Koivunen J, Siitonen A, Heinonen-Tanski H (2003) Elimination of enteric bacteria in biological–chemical wastewater treatment and tertiary filtration units. Water Res 37:690–698
Lemarchand K, Lebaron P (2003) Occurrence of salmonella spp. and cryptosporidium spp. in a French coastal watershed: relationship with fecal indicators. FEMS Microbiol Lett 218:203–209
Levantesi C, la Mantia R, Masciopinto C, Böckelmann U, Ayuso-Gabella MN, Salgot M, Tandoi V, van Houtte E, Wintgens T, Grohmann E (2010) Quantification of pathogenic microorganisms and microbial indicators in three wastewater reclamation and managed aquifer recharge facilities in Europe. Sci Total Environ 408:4923–4930
Lodder WJ, de Roda Husman AM (2005) Presence of noroviruses and other enteric viruses in sewage and surface waters in the Netherlands. Appl Environ Microbiol 71:1453–1461
Lonigro A, Pollice A, Spinelli R, Berrilli F, di Cave D, D'Orazi C, Cavallo P, Brandonisio O (2006) Giardia cysts and cryptosporidium oocysts in membrane-filtered municipal wastewater used for irrigation. Appl Environ Microbiol 72:7916–7918
McBride GB, Stott R, Miller W, Bambic D, Wuertz S (2013) Discharge-based QMRA for estimation of public health risks from exposure to stormwater-borne pathogens in recreational waters in the United States. Water Res 47:5282–5297
Medema G, Teunis P, Havelaar A, Haas C (1996) Assessment of the dose-response relationship of campylobacter jejuni. Int J Food Microbiol 30:101–111
Messner MJ, Berger P (2016) Cryptosporidium infection risk: results of new dose-response modeling. Risk Anal 36:1969–1982
Messner MJ, Berger P, Nappier SP (2014) Fractional poisson—a simple dose-response model for human norovirus. Risk Anal 34:1820–1829
Olivieri AW, Seto E (2007) Application of microbial risk assessment techniques to estimate risk due to exposure to reclaimed waters
Ottoson J, Hansen A, Westrell T, Johansen K, Norder H, Stenström TA (2006) Removal of Noro-and enteroviruses, giardia cysts, cryptosporidium oocysts, and fecal indicators at four secondary wastewater treatment plants in Sweden. Water Environ Res 78:828–834
Poté J, Goldscheider N, Haller L, Zopfi J, Khajehnouri F, Wildi W (2009) Origin and spatial–temporal distribution of faecal bacteria in a bay of Lake Geneva, Switzerland. Environ Monit Assess 154:337–348
Prevost B, Goulet M, Lucas F, Joyeux M, Moulin L, Wurtzer S (2016) Viral persistence in surface and drinking water: suitability of PCR pre-treatment with intercalating dyes. Water Res 91:68–76
Pusch D, Oh DY, Wolf S, Dumke R, Schroter-Bobsin U, Hohne M, Roske I, Schreier E (2005) Detection of enteric viruses and bacterial indicators in German environmental waters. Arch Virol 150:929–947
Rose JB (2005) Reduction of pathogens, indicator bacteria, and alternative indicators by wastewater treatment and reclamation processes. IWA Publishing,
Rose JB, Haas CN, Regli S (1991) Risk assessment and control of waterborne giardiasis. Am J Public Health 81(6):709–713.
Schoen ME, Ashbolt NJ (2010) Assessing pathogen risk to swimmers at non-sewage impacted recreational beaches. ACS Publications,
Schoen ME, Ashbolt NJ, Jahne MA, Garland J (2017) Risk-based enteric pathogen reduction targets for non-potable and direct potable use of roof runoff, stormwater, and greywater. Microbial Risk Analysis 5:32–43
Seeger EM, Braeckevelt M, Reiche N, Müller JA, Kästner M (2016) Removal of pathogen indicators from secondary effluent using slow sand filtration: optimization approaches. Ecol Eng 95:635–644. https://doi.org/10.1016/j.ecoleng.2016.06.068
Smith RJ, Twedt RM, Flanigan LK (1973) Relationships of indicator and pathogenic bacteria in stream waters Journal (Water Pollution Control Federation):1736–1745
Soller JA, Olivieri AW, Crook J, Cooper RC, Tchobanoglous G, Parkin RT, Spear RC, Eisenberg JNS (2003) Risk-based approach to evaluate the public health benefit of additional wastewater treatment. Environ Sci Technol 37:1882–1891
Soller JA, Schoen ME, Bartrand T, Ravenscroft JE, Ashbolt NJ (2010) Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination. Water Res 44:4674–4691
Soller JA, Eftim SE, Warren I, Nappier SP (2017a) Evaluation of microbiological risks associated with direct potable reuse. Microbial Risk Analysis 5:3–14
Soller JA, Schoen M, Steele JA, Griffith JF, Schiff KC (2017b) Incidence of gastrointestinal illness following wet weather recreational exposures: harmonization of quantitative microbial risk assessment with an epidemiologic investigation of surfers. Water Res (Oxford) 121:280–289
Staley C, Gordon KV, Schoen ME, Harwood VJ (2012) Performance of two quantitative PCR methods for microbial source tracking of human sewage and implications for microbial risk assessment in recreational waters. Appl Environ Microbiol 78:7317–7326
Stampi S, Varoli O, Zanetti F, De Luca G (1993) Arcobacter cryaerophilus and thermophilic campylobacters in a sewage treatment plant in Italy: two secondary treatments compared. Epidemiology Infection 110:633–639
Suptel E (1963) Pathogenesis of experimental cox sackie virus infection. Distribution of Coxsackie virus in mice after air-borne infection. Acta Virol 7:61–66
Taran-Benshoshan M, Ofer N, Dalit V-O, Aharoni A, Revhun M, Nitzan Y, Nasser AM (2015) Cryptosporidium and giardia removal by secondary and tertiary wastewater treatment. J Environ Sci Health A 50:1265–1273
Teunis P, Van den Brandhof W, Nauta M, Wagenaar J, Van den Kerkhof H, Van Pelt W (2005) A reconsideration of the campylobacter dose–response relation. Epidemiology Infection 133:583–592
Teunis PF et al (2008) Norwalk virus: how infectious is it? J Med Virol 80:1468–1476
Teunis P, Schijven J, Rutjes S (2016) A generalized dose-response relationship for adenovirus infection and illness by exposure pathway. Epidemiology Infection 144:3461–3473
USEPA (2010) Quantitative microbial risk assessment to estimate illness in freshwater impacted by agricultural animal sources of faecal contamination. US Environmental Protection Agency Office of Water, December 2010. USEPA Washington,
USEPA (2012) Recreational water quality criteria. US Environmental Protection Agency Washington, DC, Washington, DC
VanAbel N, Schoen ME, Kissel JC, Meschke JS (2017) Comparison of risk predicted by multiple norovirus dose–response models and implications for quantitative microbial risk assessment. Risk Anal 37:245–264
Wade TJ, Calderon RL, Sams E, Beach M, Brenner KP, Williams AH, Dufour AP (2006) Rapidly measured indicators of recreational water quality are predictive of swimming-associated gastrointestinal illness. Environ Health Perspect 114:24–28
Walker-Coleman L, Williams L, Pepe Menendez P (2003) Monitoring for Protozoan Pathogens in Reclaimed Water: Florida’s Requirements and Experience
Wang H, Wang T, Zhang B, Li F, Toure B, Omosa IB, Chiramba T, Abdel-Monem M, Pradhan M (2014) Water and wastewater treatment in Africa–current practices and challenges. CLEAN–Soil, Air, Water 42:1029–1035
Westrell T, Schönning C, Stenström T-A, Ashbolt N (2004) QMRA (quantitative microbial risk assessment) and HACCP (hazard analysis and critical control points) for management of pathogens in wastewater and sewage sludge treatment and reuse. Water Sci Technol 50:23–30
WHO (1999) Health based monitoring of recreational waters: the feasibility of a new approach (the" Annapolis protocol"): outcome of an expert consultation, Annapolis, USA
WHO (2011) Guidelines for drinking-water quality. Geneva: world health organization,
Wong M, Kumar L, Jenkins TM, Xagoraraki I, Phanikumar MS, Rose JB (2009) Evaluation of public health risks at recreational beaches in Lake Michigan via detection of enteric viruses and a human-specific bacteriological marker. Water Res 43:1137–1149
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Sunger, N., Hamilton, K.A., Morgan, P.M. et al. Comparison of pathogen-derived ‘total risk’ with indicator-based correlations for recreational (swimming) exposure. Environ Sci Pollut Res 26, 30614–30624 (2019). https://doi.org/10.1007/s11356-018-1881-x
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DOI: https://doi.org/10.1007/s11356-018-1881-x