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Comparison of pathogen-derived ‘total risk’ with indicator-based correlations for recreational (swimming) exposure

  • Neha Sunger
  • Kerry A. Hamilton
  • Paula M. Morgan
  • Charles N. Haas
Water Environment Protection and Contamination Treatment

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.

Keywords

QMRA Risk assessment Exposure assessment Reference pathogens Decay rates FIB 

References

  1. 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 59:348–354CrossRefGoogle Scholar
  2. 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 81:2042–2049CrossRefGoogle Scholar
  3. Anderson KL, Whitlock JE, Harwood VJ (2005) Persistence and differential survival of fecal indicator bacteria in subtropical waters and sediments. Appl Environ Microbiol 71:3041–3048CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  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 44:4692–4703CrossRefGoogle Scholar
  6. 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 74:477–484CrossRefGoogle Scholar
  7. 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 78:922–932CrossRefGoogle Scholar
  8. Betancourt WQ, Gerba CP (2016) Rethinking the significance of Reovirus in water and wastewater. Food Environ Virology 8:161–173CrossRefGoogle Scholar
  9. Brookes JD, Antenucci J, Hipsey M, Burch MD, Ashbolt NJ, Ferguson C (2004) Fate and transport of pathogens in lakes and reservoirs. Environ Int 30:741–759CrossRefGoogle Scholar
  10. Cabelli VJ (1989) Swimming-associated illness and recreational water quality criteria. Water Sci Technol 21:13–21Google Scholar
  11. Cacciò SM, De Giacomo M, Aulicino FA, Pozio E (2003) Giardia cysts in wastewater treatment plants in Italy. Appl Environ Microbiol 69:3393–3398CrossRefGoogle Scholar
  12. 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 42:3528–3538CrossRefGoogle Scholar
  13. Chaudhry RM, Nelson KL, Drewes JE (2015) Mechanisms of pathogenic virus removal in a full-scale membrane bioreactor. Environ Sci Technol 49:2815–2822CrossRefGoogle Scholar
  14. 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 14:635CrossRefGoogle Scholar
  15. 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 44:1154–1160CrossRefGoogle Scholar
  16. 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 45:257–262CrossRefGoogle Scholar
  17. Cole L, Schupp D, Erlandsen S (1989) Viability of giardia cysts suspended in lake, river, and tap water. Appl Environ Microbiol 55:1223–1229Google Scholar
  18. Coleman ME, Marks HM (2000) Mechanistic modeling of salmonellosis. Quant Microbiol 2:227–247CrossRefGoogle Scholar
  19. 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 30:517Google Scholar
  20. 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 93:529–535Google Scholar
  21. 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 80:205Google Scholar
  22. 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 91:78–86CrossRefGoogle Scholar
  23. Dietrich JP, Darby JL, Loge FJ (2009) Potential health risks associated with particles in reclaimed wastewater. J Environ Eng 135:285–290CrossRefGoogle Scholar
  24. 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,Google Scholar
  25. Dufour AP, Evans O, Behymer TD, Cantu R (2006) Water ingestion during swimming activities in a pool: a pilot study. J Water Health 4:425–430Google Scholar
  26. 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 332:855–859CrossRefGoogle Scholar
  27. 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, 1999Google Scholar
  28. 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 111:366–374CrossRefGoogle Scholar
  29. Eisenberg JN, Seto EY, Olivieri AW, Spear RC (1996) Quantifying water pathogen risk in an epidemiological framework. Risk Anal 16:549–563CrossRefGoogle Scholar
  30. 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 202:369–376CrossRefGoogle Scholar
  31. Haas CN (1983) Effect of effluent disinfection on risks of viral disease transmission via recreational water exposure. Journal (Water Pollution Control Federation) 55:1111–1116Google Scholar
  32. Haas C (2012) Quantitative Microbial Risk Assessment (QMRA) WikiGoogle Scholar
  33. Haas CN, Rose JB, Gerba C, Regli S (1993) Risk assessment of virus in drinking water. Risk Anal 13:545–552CrossRefGoogle Scholar
  34. 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 88:131–136CrossRefGoogle Scholar
  35. Haas CN, Rose JB, Gerba CP (1999) Quantitative microbial risk assessment. John Wiley & Sons,Google Scholar
  36. 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
  37. 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 71:3163–3170CrossRefGoogle Scholar
  38. He J-W, Jiang S (2005) Quantification of enterococci and human adenoviruses in environmental samples by real-time PCR. Appl Environ Microbiol 71:2250–2255CrossRefGoogle Scholar
  39. Heerden J, Ehlers M, Vivier J, Grabow W (2005) Risk assessment of adenoviruses detected in treated drinking water and recreational water. J Appl Microbiol 99:926–933CrossRefGoogle Scholar
  40. 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 45:6267–6276CrossRefGoogle Scholar
  41. 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 60:1–32Google Scholar
  42. 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 22:1547–1552CrossRefGoogle Scholar
  43. Jacangelo JG, Trussell RR (2002) International report: water and wastewater disinfection-trends, issues and practices water science and technology. Water Supply 2:147–157Google Scholar
  44. Kauppinen A, Miettinen IT (2017) Persistence of norovirus GII genome in drinking water and wastewater at different temperatures. Pathogens 6:48CrossRefGoogle Scholar
  45. 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 39:655–667CrossRefGoogle Scholar
  46. Koivunen J, Siitonen A, Heinonen-Tanski H (2003) Elimination of enteric bacteria in biological–chemical wastewater treatment and tertiary filtration units. Water Res 37:690–698CrossRefGoogle Scholar
  47. Lemarchand K, Lebaron P (2003) Occurrence of salmonella spp. and cryptosporidium spp. in a French coastal watershed: relationship with fecal indicators. FEMS Microbiol Lett 218:203–209CrossRefGoogle Scholar
  48. 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 408:4923–4930CrossRefGoogle Scholar
  49. 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 71:1453–1461CrossRefGoogle Scholar
  50. 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 72:7916–7918CrossRefGoogle Scholar
  51. 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 47:5282–5297CrossRefGoogle Scholar
  52. Medema G, Teunis P, Havelaar A, Haas C (1996) Assessment of the dose-response relationship of campylobacter jejuni. Int J Food Microbiol 30:101–111CrossRefGoogle Scholar
  53. Messner MJ, Berger P (2016) Cryptosporidium infection risk: results of new dose-response modeling. Risk Anal 36:1969–1982CrossRefGoogle Scholar
  54. Messner MJ, Berger P, Nappier SP (2014) Fractional poisson—a simple dose-response model for human norovirus. Risk Anal 34:1820–1829CrossRefGoogle Scholar
  55. Olivieri AW, Seto E (2007) Application of microbial risk assessment techniques to estimate risk due to exposure to reclaimed watersGoogle Scholar
  56. 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 78:828–834CrossRefGoogle Scholar
  57. 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 154:337–348CrossRefGoogle Scholar
  58. 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 91:68–76CrossRefGoogle Scholar
  59. 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 150:929–947CrossRefGoogle Scholar
  60. Rose JB (2005) Reduction of pathogens, indicator bacteria, and alternative indicators by wastewater treatment and reclamation processes. IWA Publishing,Google Scholar
  61. Rose JB, Haas CN, Regli S (1991) Risk assessment and control of waterborne giardiasis. Am J Public Health 81(6):709–713.Google Scholar
  62. Schoen ME, Ashbolt NJ (2010) Assessing pathogen risk to swimmers at non-sewage impacted recreational beaches. ACS Publications,Google Scholar
  63. 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 5:32–43CrossRefGoogle Scholar
  64. 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 CrossRefGoogle Scholar
  65. Smith RJ, Twedt RM, Flanigan LK (1973) Relationships of indicator and pathogenic bacteria in stream waters Journal (Water Pollution Control Federation):1736–1745Google Scholar
  66. 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 37:1882–1891CrossRefGoogle Scholar
  67. 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 44:4674–4691CrossRefGoogle Scholar
  68. Soller JA, Eftim SE, Warren I, Nappier SP (2017a) Evaluation of microbiological risks associated with direct potable reuse. Microbial Risk Analysis 5:3–14CrossRefGoogle Scholar
  69. 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) 121:280–289CrossRefGoogle Scholar
  70. 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 78:7317–7326CrossRefGoogle Scholar
  71. 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 110:633–639CrossRefGoogle Scholar
  72. Suptel E (1963) Pathogenesis of experimental cox sackie virus infection. Distribution of Coxsackie virus in mice after air-borne infection. Acta Virol 7:61–66Google Scholar
  73. 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 50:1265–1273CrossRefGoogle Scholar
  74. 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 133:583–592CrossRefGoogle Scholar
  75. Teunis PF et al (2008) Norwalk virus: how infectious is it? J Med Virol 80:1468–1476CrossRefGoogle Scholar
  76. Teunis P, Schijven J, Rutjes S (2016) A generalized dose-response relationship for adenovirus infection and illness by exposure pathway. Epidemiology Infection 144:3461–3473CrossRefGoogle Scholar
  77. 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,Google Scholar
  78. USEPA (2012) Recreational water quality criteria. US Environmental Protection Agency Washington, DC, Washington, DCGoogle Scholar
  79. 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 37:245–264CrossRefGoogle Scholar
  80. 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 114:24–28CrossRefGoogle Scholar
  81. Walker-Coleman L, Williams L, Pepe Menendez P (2003) Monitoring for Protozoan Pathogens in Reclaimed Water: Florida’s Requirements and ExperienceGoogle Scholar
  82. 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 42:1029–1035CrossRefGoogle Scholar
  83. 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 50:23–30Google Scholar
  84. WHO (1999) Health based monitoring of recreational waters: the feasibility of a new approach (the" Annapolis protocol"): outcome of an expert consultation, Annapolis, USAGoogle Scholar
  85. WHO (2011) Guidelines for drinking-water quality. Geneva: world health organization,Google Scholar
  86. 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 43:1137–1149CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of HealthWest Chester UniversityWest ChesterUSA
  2. 2.Department of Civil, Architectural, and Environmental EngineeringDrexel UniversityPhiladelphiaUSA

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