Virologica Sinica

, Volume 30, Issue 5, pp 344–353 | Cite as

Human enteric viruses–potential indicators for enhanced monitoring of recreational water quality

  • Erin Allmann Updyke
  • Zi Wang
  • Si Sun
  • Christina Connell
  • Marek Kirs
  • Mayee Wong
  • Yuanan Lu
Research Article


Recreational waters contaminated with human fecal pollution are a public health concern, and ensuring the safety of recreational waters for public use is a priority of both the Environmental Protection Agency (EPA) and the Centers for Disease Control and Prevention (CDC). Current recreational water standards rely on fecal indicator bacteria (FIB) levels as indicators of human disease risk. However present evidence indicates that levels of FIB do not always correspond to the presence of other potentially harmful organisms, such as viruses. Thus, enteric viruses are currently tested as water quality indicators, but have yet to be successfully implemented in routine monitoring of water quality. This study utilized enteric viruses as possible alternative indicators of water quality to examine 18 different fresh and offshore recreational waters on O‘ahu, Hawai‘i, by using newly established laboratory techniques including highly optimized PCR, real time PCR, and viral infectivity assays. All sample sites were detected positive for human enteric viruses by PCR including enterovirus, norovirus genogroups I and II, and male specific FRNA coliphage. A six time-point seasonal study of enteric virus presence indicated significant variation in virus detection between the rainy and dry seasons. Quantitative PCR detected the presence of norovirus genogroup II at levels at which disease risk may occur, and there was no correlation found between enteric virus presence and FIB counts. Under the present laboratory conditions, no infectious viruses were detected from the samples PCR-positive for enteric viruses. These data emphasize both the need for additional indicators for improved monitoring of water quality, and the feasibility of using enteric viruses as these indicators.


human enteric virus indicator recreational water quality Hawaii 


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  1. Allmann E, Pan L, Li L, Li D, Wang S, Lu Y. 2013. Presence of enteroviruses in recreational water in Wuhan, China. J Virol Methods, 193: 327–331.CrossRefPubMedGoogle Scholar
  2. Boehm AB, Ashbolt NJ, Colford JM, Dunbar LE, Fleming LE, Gold MA, Hansel JA, Hunter PR, Ichida AM, McGee CD, Soller JA, Weisberg SB. 2009. A sea change ahead for recreational water quality criteria. J Water Health, 7: 9–20.CrossRefPubMedGoogle Scholar
  3. Bosch A. 1998. Human enteric viruses in the water environment: a minireview. Int Microbiol, 1: 191–196.PubMedGoogle Scholar
  4. Cabelli VJ. 1983. Public health and water quality significance of viral diseases transmitted by drinking water and recreational water. Water Sci Technol, 15: 1–15.Google Scholar
  5. Calderon RL, Mood EW, Dufour AP. 1991. Health effects of swimmers and nonpoint sources of contaminated water. Int J Environ Health Res, 1: 21–31.CrossRefGoogle Scholar
  6. Colford JM, Wade TJ, Schiff KC, Wright CC, Griffith JF, Sandhu SK, Burns S, Sobsey M, Lovelace G, Weisberg SB. 2007. Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination. Epidemiology, 18: 27–35.CrossRefPubMedGoogle Scholar
  7. Connell C, Tong HI, Wang Z, Allmann E, Lu Y. 2012. New approaches for enhanced detection of enteroviruses from Hawaiian environmental waters. PLoS One, 7: e32442.PubMedCentralCrossRefPubMedGoogle Scholar
  8. Craun GF, Calderon RL, Craun MF. 2005. Outbreaks associated with recreational water in the United States. Int J Environ Health Res, 15: 243–262.CrossRefPubMedGoogle Scholar
  9. Craun MF, Craun GF, Calderon RL, Beach MJ. 2006. Waterborne outbreaks reported in the United States. J Water Health, 4: 19–30.CrossRefPubMedGoogle Scholar
  10. Dorfman M, Stoner N, Merkel M. 2004. Swimming in sewage. Natural Resources Defense Council and the Environmental Integrity Project. Avialiable: Scholar
  11. 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.PubMedGoogle Scholar
  12. Dwight RH, Baker DB, Semenza JC, Olson BH. 2004. Health effects associated with recreational coastal water use: urban versus rural California. Am J Public Health, 94: 565–567PubMedCentralCrossRefPubMedGoogle Scholar
  13. EPA 2012: Recreational Water Quality Criteria. Available: Scholar
  14. Fleisher JM, Fleming LE, Solo-Gabriele HM, Kish JK, Sinigalliano CD, Plano L, Elmir SM, Wang JD, Withum K, Shibata T. 2010. The BEACHES Study: health effects and exposures from non-point source microbial contaminants in subtropical recreational marine waters. Int J Epidemiol, 39: 129–1298.CrossRefGoogle Scholar
  15. Fleming LE, Solo GH, Elmir S, Shibata T, Squicciarini D, Quirino W, Arguello M, Van de Bogart G. 2004. A Pilot Study of Microbial Contamination of Subtropical Recreational Waters. Fla J Environ Health, 184: 29.PubMedCentralPubMedGoogle Scholar
  16. Fong TT, Lipp EK. 2005. Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev, 69: 357–371.PubMedCentralCrossRefPubMedGoogle Scholar
  17. Fujioka R, Sian-Denton C, Borja M, Castro J, Morphew K. 1998. Soil: the environmental source of Escherichia coli and Enterococci in Guam's streams. J Appl Microbiol, 85: 83S–89S.CrossRefGoogle Scholar
  18. Fujioka RS, Byappanahalli MN. 1996. Assessing the applicability of USEPA recreational water quality standards to Hawaii and other tropical islands. Available: Scholar
  19. Fujioka RS, Tenno K, Kansako S. 1988. Naturally occurring fecal coliforms and fecal streptococci in Hawaii's freshwater streams. Toxicity Assessment, 3: 613–630.CrossRefGoogle Scholar
  20. Gerba C, Wallis C, Melnick J. 1975. Viruses in water: the problem, some solutions. Environ Sci Technol, 9: 1122–1126.CrossRefGoogle Scholar
  21. Gerba CP, Goyal SM, LaBelle RL, Cech I, Bodgan GF. 1979. Failure of indicator bacteria to reflect the occurrence of enteroviruses in marine waters. Am J Public Health, 69: 1116–1119.PubMedCentralCrossRefPubMedGoogle Scholar
  22. Hlavsa MC, Brunkard JM. 2011. Surveillance for Waterborne Disease Outbreaks and Other Health Events Associated with Recreational Water—United States, 2007-2008. US Department of Health and Human Services, Centers for Disease Control and Prevention.Google Scholar
  23. Ijzerman MM, Dahling DR, Fout GS. 1997. A method to remove environmental inhibitors prior to the detection of waterborne enteric viruses by reverse transcription-polymerase chain reaction. J Virol Methods, 63: 145–153.CrossRefPubMedGoogle Scholar
  24. Jiang SC, Chu W. 2004. PCR detection of pathogenic viruses in southern California urban rivers. J Appl Microbiol, 97: 17–28.CrossRefPubMedGoogle Scholar
  25. Katayama H, Shimasaki A, Ohgaki S. 2002. Development of a virus concentration method and its application to detection of enterovirus and Norwalk virus from coastal seawater. Appl Environ Microbiol, 68: 1033–1039.PubMedCentralCrossRefPubMedGoogle Scholar
  26. Lees D. 2000. Viruses and bivalve shellfish. Int J Food Microbiol, 59: 81–116.CrossRefPubMedGoogle Scholar
  27. Lopez-Torres AJ, Hazen TC, Toranzos GA. 1987. Distribution and in situ survival and activity of Klebsiella pneumoniae and Escherichia coli in a tropical rain forest watershed. Curr Microbiol, 15: 213–218.CrossRefGoogle Scholar
  28. Okoh AI, Sibanda T, Gusha SS. 2010. Inadequately treated wastewater as a source of human enteric viruses in the environment. Int J Env Res Pub He, 7: 2620–2637.CrossRefGoogle Scholar
  29. Pusch D, Oh D-Y, Wolf S, Dumke R, Schröter-Bobsin U, Höhne M, Röske I, Schreier E. 2005. Detection of enteric viruses and bacterial indicators in German environmental waters. Arch Virol, 150: 929–947.CrossRefPubMedGoogle Scholar
  30. Schwab KJ, De Leon R, Sobsey MD. 1996. Immunoaffinity concentration and purification of waterborne enteric viruses for detection by reverse transcriptase PCR. Appl Environ Microbiol, 62: 2086–2094.PubMedCentralPubMedGoogle Scholar
  31. Shuval H. 2003. Estimating the global burden of thalassogenic diseases: human infectious diseases caused by wastewater pollution of the marine environment. J Water Health, 1: 53–64.PubMedGoogle Scholar
  32. Sinclair R, Jones E, Gerba C. 2009. Viruses in recreational waterborne disease outbreaks: a review. J Appl Microbiol, 107: 1769–1780.CrossRefPubMedGoogle Scholar
  33. Sinigalliano CD, Fleisher JM, Gidley ML, Solo-Gabriele HM, Shibata T, Plano LR, Elmir SM, Wanless D, Bartkowiak J, Boiteau R. 2010. Traditional and molecular analyses for fecal indicator bacteria in non-point source subtropical recreational marine waters. Water Res, 44: 3763–3772.PubMedCentralCrossRefPubMedGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. The Hawaii Department of Health. 2012. 2008/2010 State of Hawaii Water Quality Monitoring and Assessment Report. Honolulu, Hawaii.Google Scholar
  36. Tong HI, Connell C, Boehm AB, Lu Y. 2011. Effective detection of human noroviruses in Hawaiian waters using enhanced RTPCR methods. Water Res, 45: 5837–5848.CrossRefPubMedGoogle Scholar
  37. Tong HI, Lu Y. 2011. Effective detection of human adenovirus in Hawaiian waters using enhanced PCR method. Virol J, 8: 57.PubMedCentralCrossRefPubMedGoogle Scholar
  38. Trujillo AA, McCaustland KA Zheng DP, Hadley LA, Vaughn G, Adams SM, Ando T, Glass RI, Monroe SS. 2006. Use of TaqMan real-time reverse transcription-PCR for rapid detection, quantification, and typing of norovirus. J Clin Microbiol, 44: 1405–1412.PubMedCentralCrossRefPubMedGoogle Scholar
  39. United States Environmental Protection Agency. 2012. EPA’s BEACH Report: 2011 Swimming Season.Google Scholar
  40. United States Environmental Protection Agency. 2012. Recreational Water Quality Criteria. Available: Scholar
  41. Viau EJ, Goodwin KD, Yamahara KM, Layton BA, Sassoubre LM, Burns SL, Tong H-I, Wong SH, Lu Y, Boehm AB. 2011. Bacterial pathogens in Hawaiian coastal streams—associations with fecal indicators, land cover, and water quality. Water Res, 45: 3279–3290.CrossRefPubMedGoogle Scholar
  42. Wade TJ, Pai N, Eisenberg JN, Colford JM. 2003. Do US Environmental Protection Agency water quality guidelines for recreational waters prevent gastrointestinal illness? A systematic review and meta-analysis. Environ Health Perspect, 111: 1102.CrossRefPubMedGoogle Scholar
  43. Wade TJ, Sams E, Brenner KP, Haugland R, Chern E, Beach M, Wymer L, Rankin CC, Love D, Li Q. 2010. Rapidly measured indicators of recreational water quality and swimming-associated illness at marine beaches: a prospective cohort study. Environ Health-Glob, 9: 1–14.CrossRefGoogle Scholar
  44. Wang Z, Sun S, Connell C, Lu Y. 2014. Effective Recovery of Infectious Human Enterovirus from Environmental Waters for Their Application for Water Quality Monitoring. Global Health Journal, 1: 37–45.Google Scholar
  45. Xagoraraki I, Kuo DH, Wong K, Wong M, Rose JB. 2007. Occurrence of human adenoviruses at two recreational beaches of the great lakes. Appl Environ Microb, 73: 7874–7881.CrossRefGoogle Scholar

Copyright information

© Wuhan Institute of Virology, CAS and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Erin Allmann Updyke
    • 1
  • Zi Wang
    • 1
  • Si Sun
    • 1
  • Christina Connell
    • 1
  • Marek Kirs
    • 2
  • Mayee Wong
    • 2
  • Yuanan Lu
    • 1
  1. 1.Department of Public Health SciencesUniversity of Hawai‘i at MānoaHawaiiUSA
  2. 2.Water Resources Research CenterUniversity of Hawai‘i at MānoaHawaiiUSA

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