Cryptosporidium and Giardia in tropical recreational marine waters contaminated with domestic sewage: Estimation of bathing-associated disease risks

Marine Pollution Bulletin

Volumn 85, Issue 1, 2014, Pages 268-273

  Betancourt, Walter Q ^a   Duarte, Diana C ^a   Vásquez, Rosa C ^a   Gurian, Patrick L ^b  

^a INSTITUTO VENEZOLANO DE INVESTIGACIONES CIENTÍFICAS   (Venezuela)

^b Drexel University   (United States)

Author keywords

Marine waters; Parasites; Recreation; Risks; Sewage; Tropics

Indexed keywords

MONTE CARLO METHODS; PROBABILITY DISTRIBUTIONS; PROTOZOA; RISKS; SEWAGE; TROPICS; UNCERTAINTY ANALYSIS; WATER POLLUTION; WATER QUALITY;

CLOSTRIDIUM PERFRINGENS; DOSE-RESPONSE MODELING; ENVIRONMENTAL SURVEILLANCE; MARINE WATERS; PARASITES; RECREATION; RECREATIONAL WATER QUALITY; WATER QUALITY DETERIORATION;

RISK PERCEPTION;

4',6 DIAMIDINO 2 PHENYLINDOLE; PROPIDIUM IODIDE; SEA WATER; FRESH WATER; SEWAGE;

DOSE-RESPONSE RELATIONSHIP; HEALTH RISK; INFECTIOUS DISEASE; MARINE POLLUTION; MONTE CARLO ANALYSIS; PARASITE; PATHOGEN; PROTOZOAN; RECREATIONAL FACILITY; SEWAGE; UNCERTAINTY ANALYSIS; WATER QUALITY;

ADULT; ARTICLE; BACTEROIDALES; CHILD; CLOSTRIDIUM; CLOSTRIDIUM COCCOIDES; CLOSTRIDIUM PERFRINGENS; CONTROLLED STUDY; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; DETERIORATION; ENTEROCOCCUS; ENVIRONMENTAL IMPACT ASSESSMENT; GENETIC MARKER; GIARDIA; GIARDIASIS; HEALTH HAZARD; HUMAN; MARINE ENVIRONMENT; MONTE CARLO METHOD; NOMARSKI INTERFERENCE CONTRAST MICROSCOPE; NONHUMAN; PARASITOSIS; PATHOGENESIS; PROBABILITY; RECREATION; RISK ASSESSMENT; SEA POLLUTION; SEWAGE; SWIMMING; TROPICS; WATER CONTAMINATION; WATER QUALITY; ANIMAL; ENVIRONMENTAL MONITORING; GEOGRAPHY; ISOLATION AND PURIFICATION; MICROBIOLOGY; PARASITOLOGY; PROCEDURES; RISK; VENEZUELA;

BACTEROIDALES; CLOSTRIDIUM COCCOIDES; CLOSTRIDIUM PERFRINGENS; CRYPTOSPORIDIUM; GIARDIA; PROTOZOA;

ANIMALS; BATHING BEACHES; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; ENVIRONMENTAL MONITORING; FRESH WATER; GEOGRAPHY; GIARDIA; GIARDIASIS; HUMANS; MONTE CARLO METHOD; RECREATION; RISK; RISK ASSESSMENT; SEWAGE; VENEZUELA; WATER MICROBIOLOGY;

EID: 84905748777     PISSN: 0025326X     EISSN: 18793363     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2014.05.059     Document Type: Article

References (43)

1. Abhelzaher A.M., Wright M.E., Ortega C., Solo-Gabriele H.M., Miller G., Elmir S., Newman X., Shih P., Bonilla J.A., Bonilla T.D., et al. Presence of pathogens and indicator microbes at a non-point source subtropical recreational marine beach. Appl. Environ. Microbiol. 2010, 76:724-732.
2. Betancourt W.Q., Mena K.D. Assessment of waterborne protozoan passage through conventional drinking water treatment process in Venezuela. J. Wat. Health 2012, 10:324-336.
3. Betancourt W.Q., Querales L., Sulbaran Y.F., Rodriguez-Diaz J., Caraballo L., Pujol F.H. Molecular characterization of sewage-borne pathogens and detection of sewage markers in an urban stream in Caracas, Venezuela. Appl. Environ. Microbiol. 2010, 76:2023-2026.
4. Caccio S.M., Thompson R.C.A., McLauchlin J., Smith H.W. Unravelling Cryptosporidium and Giardia epidemiology. Trends Parasitol 2005, 21:430-437.
5. Dyble J., Bienfang P., Dusek E., Hitchcock G., Holland F., Laws E., Lerczak J., McGillicuddy D.J., Minnett P., Moore S.K., O'Kelly C., Solo-Gabriele H., Wang J.D. Environmental controls, oceanography and population dynamics of pathogens and harmful algal blooms: connecting sources to human exposure. Environ. Health 2008, 7(Suppl. 2):S5. 10.1186/1476-069X-7-S2-S5.
6. Enger, K., 2013a. Giardia duodenalis: Dose Response Models, QMRA Wiki, available online at http://qmrawiki.msu.edu/index.php?title=Giardia_duodenalis%3A_Dose_Response_Models#1,(accessed 16.05.2014).
7. Enger, K., 2013b. Cryptosporidium parvum and Cryptosporidium hominis: dose Response Models, QMRA Wiki, available online at: http://qmrawiki.msu.edu/index.php?title=Cryptosporidium_parvum_and_Cryptosporidium_hominis%3A_Dose_Response_Models#Summary_of_Data, (accessed 16.05.2014).
8. Fleisher J.M., Kay D., Wyer M.D., Godfree A.F. Estimates of the severity of illnesses associated with bathing in marine recreational waters contaminated with domestic sewage. Int. J. Epidemiol. 1998, 27:722-726.
9. Fleming L.E., Broad K., Clement A., Dewailly E., Elmir S., Knap A., Pomponi S.A., Smith S., Solo Gabriele H., Walsh P. Oceans and human health: emerging public health risks in the marine environment. Mar. Poll. Bull. 2006, 53:545-560.
10. Fujioka R. Monitoring coastal marine waters for spore-forming bacteria of fecal and soil origin to determine point from non-point source of pollution. Wat. Sci. Technol. 2001, 44:181-188.
11. Graczyk T.K., Sunderland D., Awantang G.N., Mashinski Y., Lucy F.E., Graczyk Z., Chomicz L., Breysse P.N. Relationships among bather density, levels of human waterborne pathogens, and fecal coliform counts in marine recreational beach water. Parasitol. Res. 2010, 106:1103-1108.
12. Gerba C.P. Virus occurrence and survival in the environmental waters. Human Viruses in Water 1999, Elsevier, Amsterdam, The Netherlands. A. Bosh (Ed.).
13. Haas C.N., Rose J.B., Gerba C.P. Conducting the dose-response assessment. Quant. Microb. Risk Assessment 1999, John Wiley & Sons, New York. C.N. Haas, J.B. Rose, C.P. Gerba (Eds.).
14. Johnson D.C., Reynolds K.A., Gerba C.P., Pepper I.L., Rose J.B. Detection of Giardia and Cryptosporidium in marine waters. Wat. Sci. Technol. 1995, 31:439-442.
15. Karydis M., Kitsiou D. Marine water quality monitoring: a review. Mar. Poll. Bull. 2013, 77:23-36.
16. Knap A., Dewailly E., Furgal C., et al. Indicators of ocean health and human health: a research framework. Environ. Health Perspect. 2002, 110:839-845.
17. Matsuki T., Watanabe K., Fujimoto J., Takada T., Tanaka R. Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl. Environ. Microbiol. 2004, 70:7220-7228.
18. McLellan S.L., Ryan J., Newton R.J., Vandewalle J.L., Shanks O.C., Huse S.M., Murat E.A., Sogin M.L. Sewage reflects the distribution of human faecal Lachnospiraceae. Environ. Microbiol. 2013, 15:2213-2227.
19. McOliver C.C., Lemerman H.B., Silbergeld E.K., Moore R.D., Graczyk T.K. Risk of recreational water exposure to waterborne pathogens among persons with HIV/AIDS in Baltimore, Maryland. Am. J. Public Health 2009, 99:1116-1122.
20. Medema G.J., Schijven J.F. Modeling the sewage discharge and dispersion of Cryptosporidium and Giardia in surface water. Wat. Res. 2001, 35:4307-4316.
21. Messer J.W., Dufour A.P. A rapid, specific membrane filtration procedure for enumeration of enterococci in recreational water. Appl. Environ. Microbiol. 1998, 64:678-680.
22. National Research Council (1993) Managing wastewater in coastal urban areas. National Academy Press, Washington, DC.
23. Nichols R.A.B., Campbell B.M., Smith H.V. Molecular fingerprinting of Cryptosporidium oocysts during water monitoring. Appl. Environ. Microbiol. 2006, 72:5428-5436.
24. Noble R.T., Blackwood A.D., Griffith J.F., McGee C.D., Weisberg S.B. Comparison of rapid quantitative PCR-based and conventional culture-based methods for enumeration of Enterococcus spp. and Escherichia coli in recreational waters. Appl. Environ. Microbiol. 2010, 76:7437-7443.
25. Overstreet R.M. Waterborne parasitic diseases in ocean. Infectious Diseases: Selected Entries from the Encyclopedia of Sustainability Science and Technology 2013, Springer, Science + Business Media, New York, p. 1-90.
26. Quintero-Betancourt W., Gennaccaro A.L., Scott T.M., Rose J.B. Assessment of methods for detection of infectious Cryptosporidium oocysts and Giardia cysts in reclaimed effluents. Appl. Environ. Microbiol. 2003, 69:5380-5388.
27. Robertson L.J., Hermasen J.L., Gjerde B.K. Occurrence of Cryptosporidium oocysts and Giardia cysts in sewage in Norway. Appl. Environ. Microbiol. 2006, 72:5297-5303.
28. Seurinck S., Defoirdt T., Verstraete W., Siciliano S.D. Detection and quantification of the human-specific HF183 Bacteroides 16S rRNA genetic marker with real-time PCR for assessment of human faecal pollution in freshwater. Environ. Microbiol. 2005, 7:249-259.
29. Shuval H. Estimating the global burden of thalasogenic diseases: human infections diseases caused by wastewater pollution of the marine environment. J. Wat. Health 2003, 1:53-64.
30. Stewart J.R., Gast R.J., Fujioka R.S., Solo-Gabriele H.M., Scott M.J., Amaral-Zettler L.A., del Castillo E., Polz M.F., Collier T.K., Strom M.S., Sinigalliano C.D., Moeller P.D.R., Fredrick H.A. The coastal environment and human health: microbial indicators, pathogens, sentinels and reservoirs. Environ. Health 2008, 7(Suppl 2):1-14. doi: 10.1186/1476-069X-7-S2-S3.
31. Sulaiman I.M., Fayer M.R., Bern C., Gilman R.H., Trout J.M., Schantz P.M., Das P., Lal A.A., Xiao L. Triosephosphate isomerase gene characterization and potential zoonotic transmission of multispecies Giardia duodenalis. Emerg. Infect. Dis. 2003, 9:1444-1452.
32. Tap J., Mondot S., Levenez F., Pelletier E., Caron C., Furet J.P., Ugarte E., Munoz-Tamayo R., Paslier D.L., Nalin R., Dore J., Leclerc M. Towards the human intestinal microbiota phylogenetic core. Environ. Microbiol. 2009, 11:2574-2584.
33. Tibbetts J. Coastal cities: living on the edge. Environ. Health Perspect. 2002, 110(11):A674-A681.
34. Tiwari G.N. Solar energy. Fund. Des. Mod. Appl. 2002, Alpha Science International Ltd, United Kingdom. G.N. Tiwari (Ed.).
35. Trujillo A.P., Thurman H.V. The coastal ocean. Essentials of Oceanography 2008, Pearson Prentice Hall, New Jersey. A.P. Trujillo (Ed.).
36. UNEP -UCR/CEP., (2010). Updated CEP Technical Report No. 33 Land-based Sources and Activities.
37. U.S. EPA., (2011). Exposure Factors Handbook: 2011 Edition (Final). (EPA/600/R-09/052F). Washington, DC.
38. U.S. EPA., (2012). 2012 Recreational Water Quality Criteria, Office of Water, U.S. EPA, EPA-820-F-12-061, Washington, DC, available online at: (accessed 16.05.2014). http://water.epa.gov/scitech/swguidance/standards/criteria/health/recreation/upload/factsheet2012.pdf.
39. Van Dyke M.I., Ong C.S., Prystajecky N.A., Isaac-Renton J.L., Huck P.M. Identifying host sources, human health risk and indicators of Cryptosporidium and Giardia in a Canadian watershed influenced by urban and rural activities. J. Wat. Health 2012, 10:311-323.
40. Viau E.J., Lee D., Boehm A.B. Swimmer risk of gastrointestinal illness from exposure to tropical coastal waters impacted by terrestrial dry-weather runoff. Environ. Sci. Technol. 2011, 45:7158-7165.
41. Vierheilig J., Frick C., Mayer R.E., Kirschner A.K.T., Reischer G.H., Derx J., Mach R.L., Sommer R., Farnleitner A.H. Clostridium perfringens is not suitable for the indication of fecal pollution from ruminant wildlife but is associated with excreta from non-herbivorous animals and human sewage. Appl. Environ. Microbiol. 2013, 79:5089-5092.
42. World Health Organization (WHO), 2005. Water Recreation and Disease. Plausibility of associated Infections: Acute Effects, Sequelae and Mortality by Kathy Pond. Published by IWA Publishing, London, UK. ISBN: 18433906.
43. Xiao L., Singh A., limor J., Graczyk T.K., Gradus S., Lal A. Molecular characterization of Cryptosporidium oocysts in samples of raw surface water and wastewater. Appl. Environ. Microbiol. 2001, 67:1097-1101.