Contribution of treated wastewater to the contamination of recreational river areas with Cryptosporidium spp. and Giardia duodenalis

Water Research

Volumn 42, Issue 13, 2008, Pages 3528-3538

  Castro Hermida, José Antonio ^a   García Presedo, Ignacio ^a   Almeida, André ^b   González Warleta, Marta ^a   Da Costa, José Manuel Correia ^b   Mezo, Mercedes ^a  

^a Centro de Investigacions Agrarias de Mabegondo   (Spain)

^b NATIONAL INSTITUTE OF HEALTH   (Portugal)

Author keywords

Cryptosporidium spp.; Giardia duodenalis; Public health; Recreational river areas; Spain; Wastewater; Water quality

Indexed keywords

CHROMIUM COMPOUNDS; EFFLUENT TREATMENT; ENVIRONMENTAL PROTECTION AGENCY; PROTOZOA; PUBLIC HEALTH; RIVER POLLUTION; RNA; WASTEWATER; WASTEWATER TREATMENT; WATER QUALITY;

CRYPTOSPORIDIUM HOMINIS; CRYPTOSPORIDIUM PARVUM; CRYPTOSPORIDIUM SPP; GIARDIA DUODENALIS; RECREATIONAL RIVER AREAS; SPAIN; US ENVIRONMENTAL PROTECTION AGENCY; WASTEWATER TREATMENT PLANTS;

EFFLUENTS;

RIBOSOME RNA;

BEACH; FLAGELLATE; PROTOZOAN; RECREATIONAL FACILITY; RIVER POLLUTION; WASTEWATER; WATER QUALITY; WATER TREATMENT;

ARTICLE; AUTUMN; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM HOMINIS; CRYPTOSPORIDIUM PARVUM; CYST (RESTING STAGE); EFFLUENT; GENE AMPLIFICATION; GENE SEQUENCE; GENOTYPE; GIARDIA DUODENALIS; PRIORITY JOURNAL; RIVER; SEASHORE; SPRING; SUMMER; WASTE WATER; WATER ANALYSIS; WATER CONTAMINATION; WATER SAMPLING; WINTER;

AUSTRALASIA; AUSTRALIA; GLIKSON STRUCTURE; WESTERN AUSTRALIA;

CRYPTOSPORIDIUM; CRYPTOSPORIDIUM ANDERSONI; CRYPTOSPORIDIUM HOMINIS; CRYPTOSPORIDIUM PARVUM; GIARDIA INTESTINALIS;

EID: 54049101618     PISSN: 00431354     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.watres.2008.05.001     Document Type: Article

References (61)

1. Adam, R.D., 2001. Biology of Giardia lamblia. Clin. Microbial. Rev. 14, 447-475.
2. Anderson, M.A., Stewart, M.H., Yates, M.V., Gerba, C.P., 1998. Modeling the impact of body-contact recreation on pathogen concentrations in a source drinking water reservoir. Water Res. 32, 3293-3306.
3. Brookes, J.D., Antenucci, J., Hipsey, M., Burch, M.D., Ashbolt, N.J., Ferguson, C., 2004. Fate and transport of pathogens in lakes and reservoirs. Environ. Int. 30, 741-759.
4. Brookes, J.D., Hipsey, M., Burch, M.D., Regel, R.H., Linden, L.G., Ferguson, C., 2005. Relative value of surrogate indicators for detecting pathogens in lakes and reservoirs. Environ. Sci. Technol. 39, 8614-8621.
5. Bukhari, Z., Smith, H.V., Sykes, N., Humphreys, S.W., Paton, C.A., Girdwood, R.W.A., Fricker, C.R., 1997. Occurrence of Cryptosporidium spp. oocysts and Giardia cysts in sewage influents and effluents from treatment plants in England. Water Sci. Technol. 35, 385-390.
6. Cacciò, S.M., De Giacomo, M., Aulicino, F.A., Pozio, E., 2003. Giardia cysts in wastewater treatment plants in Italy. Appl. Environ. Microbiol. 69, 3393-3398.
7. Cacciò , S.M., De Giacomo, M., Pozio, E., 2002. Sequence analysis of the β-giardin gene and development of a polymerase chain reaction-restriction fragment length polymorphism assay to genotype Giardia duodenalis cysts from human faecal samples. Int. J. Parasitol. 32, 1023-1030.
8. Carmena, D., Aguinagalde, X., Zigorraga, C., Fernández-Crespo, J.C., Ocio, J.A., 2007. Presence of Giardia cysts and Cryptosporidium oocysts in drinking water supplies in northern Spain. J. Appl. Microbiol. 102, 619-629.
9. Casson, L.W., Sorber, C.A., Sykora, J.L., Gavaghan, P.D., Shapiro, M.A., Jakubowski, W., 1990. Giardia in wastewater - effect of treatment. Water Pollut. Control Fed. Res. J. 62, 670-675.
10. Castro-Hermida, J.A., Delafosse, A., Pors, I., Ares-Mazás, E., Chartier, C., 2005. Giardia duodenalis and Cryptosporidium parvum infections in adult goats and their implications for neonatal kids. Vet. Rec. 157, 623.
11. Castro-Hermida, J.A., Almeida, A., González-Warleta, M., Correia da Costa, J.M., Mezo, M., 2006a. Prevalence and preliminary genetic characterization of Cryptosporidium spp. isolated from asymptomatic heifers in Galicia (NW, Spain). J. Eukariot. Microbiol. 53, S22-S23.
12. Castro-Hermida, J.A., Almeida, A., González-Warleta, M., Correia da Costa, J.M., Mezo, M., 2006b. Prevalence and preliminary genetic analysis of Giardia isolated from adult sheep in Galicia (NW, Spain). J. Eukariot. Microbiol. 53, S172-S173.
13. Castro-Hermida, J.A., Almeida, A., González-Warleta, M., Correia da Costa, J.M., Rumbo-Lorenzo, C., Mezo, M., 2007a. Occurrence of Cryptosporidium parvum and Giardia duodenalis in healthy adult domestic ruminants. Parasitol. Res. 101, 1443-1448.
14. Castro-Hermida, J.A., González-Warleta, M., Mezo, M., 2007b. Natural infection by Cryptosporidium parvum and Giardia duodenalis in sheep and goats in Galicia (NW Spain). Small Rumin. Res. 72, 96-100.
15. Chappell, C.L., Okhuysen, P.C., Langer-Curry, R., Widmer, G., Akiyoshi, D.E., Tanriverdi, S., Tzipori, S., 2006. Cryptosporidium hominis: experimental challenge of healthy adults. Am. J. Trop. Med. Hyg. 75, 851-857.
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, 257-262.
17. Center of Disease Control and Prevention, 2006. Fact sheet - crypto-protection against recreational water illness 〈http://www.cdc.gov/ healthyswimming/cryptofacts.htm〉 [online].
18. Craun, G.F., Calderon, R.L., Craun, M.F., 2005. Outbreaks associated with recreational water in United States. Int. J. Environ. Health Res. 15, 243-262.
19. Dai, X., Boll, J., 2006. Settling velocity of Cryptosporidium parvum and Giardia lamblia. Water Res. 40, 1321-1325.
20. Directive 92/43/EEC., 1992. Council of the European Communities. Directive on the conservation of natural habitats and of wild fauna and flora. J. Off. Union Eur. L 206, 0007-0050.
21. DuPont, H.L., Chappell, C.L., Sterling, C.R., Okhuysen, P.C., Rose, J.B., Jakubowski, W., 1995. The infectivity of Cryptosporidium parvum in healthy volunteers. N. Engl. J. Med. 332, 855-859.
22. Enriquez, C., Nwachuku, N., Gerba, C.P., 2001. Direct exposure to animal enteric pathogens. Rev. Environ. Health 16, 117-131.
23. Fayer, R., 2004. Cryptosporidium: a water-borne zoonotic parasite. Vet. Parasitol. 126, 37-56.
24. Fayer, R., Morgan, U., Upton, S.J., 2000. Epidemiology of Cryptosporidium: transmission, detection and identification. Int. J. Parasitol. 30, 1305-1322.
25. Giangaspero, A., Berrilli, F., Brandonisio, O., 2007. Giardia and Cryptosporidium and public health: the epidemiological scenario from the Italian perspective. Parasitol. Res. 101, 1169-1182.
26. Giovanni, G.D., Betancourt, W.Q., Hernandez, J., Assadian, N.W., Flores Margez, J.P., Jaramillo Lopez, E., 2006. Investigation of potential zooanthroponotic transmission of cryptosporidiosis and giardiosis through agricultural use of reclaimed wastewater. Int. J. Environ. Health Res. 16, 405-418.
27. Gómez-Couso, H., Méndez-Hermida, F., Castro-Hermida, J.A., Ares-Mazás, E., 2005. Giardia in shellfish-farming areas: detection in mussels, river water and waste waters. Vet. Parasitol. 133, 13-18.
28. Gómez-Couso, H., Méndez-Hermida, F., Castro-Hermida, J.A., Ares-Mazás, E., 2006. Cryptosporidium contamination in harvesting areas of bivalve molluscs. J. Food Protect. 69, 185-190.
29. Graczyk, T.K., Lucy, F.E., Tamang, L., Miraflor, A., 2007. Human enteropathogen load in activated sewage sludge and corresponding sewage end products. Appl. Environ. Microbiol. 73, 2013-2015.
30. Hancock, D., Besser, T., Lejeune, J., Davis, M., Rice, D., 2001. The control of VTEC in the animal reservoir. Int. J. Food Microbiol. 66, 71-78.
31. Hashimoto, A., Hirata, T., Kunikane, S., 2001. Occurrence of Cryptosporidium oocysts and Giardia cysts in a conventional water purification plant. Water Sci. Technol. 43, 89-92.
32. Indest, K., 2003. Interim guidance on assessing the risk posed by pathogens associated with dredged material (no. ERDC/TN EEDP-01-49).
33. Isaac-Renton, J., Moorehead, W., Ross, A., 1996. Longitudinal studies of Giardia contamination in two community drinking water supplies: cysts levels, parasite viability, and health impact. Appl. Environ. Microbiol. 62, 47-54.
34. Karanis, P., Papadopoulou, C., Kimua, A., Economou, E., Kourenti, C., Sakkas, H., 2002. Cryptosporidium and Giardia in natural, drinking and recreational water of northwestern Greece. Acta Hydrochim. Hydrobiol. 30, 49-58.
35. Lim, Y.A.L., Hafiz, W., Nissapatorn, V., 2007. Reduction of Cryptosporidium and Giardia by sewage treatment processes. Trop. Biomed. 24, 95-104.
36. McCuin, R.M., Clancy, J.L., 2003. Modifications to United States environmental protection agency methods 1622 and 1623 for detection of Cryptosporidium oocysts and Giardia cysts in water. Appl. Environ. Microbiol. 69, 267-274.
37. Meyer, E.A., Jarroll, E.J., 1980. Giardiasis. Am. J. Epidemiol. 111, 1-12.
38. Montemayor, M., Valero, F., Cofre, J., Lucena, F., 2005. Occurrence of Cryptosporidium spp. oocysts in raw and treated sewage and river water in north-eastern Spain. J. Appl. Microbiol. 99, 1455-1462.
39. Perz, J.F., LeBlancq, S.M., 2001. Cryptosporidium parvum infection involving novel genotypes in wildlife from lower New York State. Appl. Environ. Microbiol. 67, 1154-1162.
40. Quintero-Betancourt, W., Gennaccaro, A.L., Scott, T.M., Rose, J.B., 2003. Assessment of methods for detection of infectious Cryptosporidium oocysts and Giardia cysts in reclaimed effluents. Appl. Environ. Microbiol. 69, 5380-5388.
41. Reynolds, K.A., Mena, K.D., Gerba, C.P., 2008. Risk of waterborne illness via drinking water in the United States. Rev. Environ. Contam. Toxicol. 192, 117-158.
42. Robertson, L.J., Gjerde, B.K., 2001. Occurrence of Cryptosporidium oocysts and Giardia cysts in raw waters in Norway. Scand. J. Public Health 29, 200-207.
43. Robertson, L.J., Paton, C.A., Campbell, A.T., Smith, P.G., Jackson, M.H., Gilmour, R.A., Black, S.E., Stevenson, D.A., Smith, H.V., 2000. Giardia cysts and Cryptosporidium oocysts at sewage treatment works in Scotland, UK. Water Res. 34, 2310-2322.
44. Robertson, L.J., Hermansen, L., Gjerde, B.K., 2006. Occurrence of Cryptosporidium oocysts and Giardia cysts in sewage in Norway. Appl. Environ. Microbiol. 72, 5297-5303.
45. Rueker, N.J., Braithwaite, S.L., Topp, E., Edge, T., Lapen, D.R., Wilkes, G., Robertson, W., Medeiros, D., Sensen, C.W., Neumann, N.F., 2007. Tracking host sources of Cryptosporidium spp. in raw water for improved health risk assessment. Appl. Environ. Microbiol. 73, 3945-3957.
46. Ryan, U., Xiao, L., Read, C., Zhou, L., Lal, A.A., Pavlasek, I., 2003. Identification of novel Cryptosporidium genotypes from the Czech Republic. Appl. Environ. Microbiol. 69, 4302-4307.
47. Searcy, K.E., Packman, A.I., Atwill, E.R., Harter, T., 2005. Association of Cryptosporidium parvum with suspended particles: impact on oocyst sedimentation. Appl. Environ. Microbiol. 71, 1072-1078.
48. Slifko, T.R., Smith, H.V., Rose, J.B., 2000. Emerging parasite zoonoses associated with water and food. Int. J. Parasitol. 30, 1379-1393.
49. Smith, H.V., Rose, J.B., 1990. Waterborne cryptosporidiosis. Parasitol. Today 6, 8-12.
50. Smith, H.V., Cacciò, S.M., Cook, N., Nichols, R.A.B., Tait, A., 2007. Cryptosporidium and Giardia as foodborne zoonoses. Vet. Parasitol. 149, 29-40.
51. Sterling, C.R., 1990. Waterborne cryptosporidiosis. In: Dubey, J.P., Speer, C.A., Fayer, R. (Eds.), Cryptosporidiosis of Man and Animals. CRC Press, Boca Ratón, FL, pp. 51-58.
52. Sunderland, D., Graczyk, T.K., Tamang, L., Breysse, P.N., 2007. Impact of bathers on levels of Cryptosporidium parvum oocysts and Giardia lamblia cysts in recreational beach waters. Water Res. 41, 3483-3489.
53. Tamburrini, A., Pozio, E., 1999. Long-term survival of Cryptosporidium parvum oocysts in seawater and in experimentally infected mussels (Mytilus galloprovincialis). Int. J. Parasitol. 29, 711-715.
54. Thompson, R.C.A., 2000. Giardiasis as a re-emerging infectious disease and its zoonotic potential. Int. J. Parasitol. 30, 1259-1267.
55. US Environmental Protection Agency, 2001. Method 1623: Cryptosporidium and Giardia in water by filtration/IMS/FA. EPA 821-R-01-025. Office of Ground Water and Drinking Water Technical Support Center, US Environmental Protection Agency, Washington, DC.
56. Villacorta-Martínez de Maturana, I., Ares-Mazás, M.E., Durán-Oreiro, D., Lorenzo-Lorenzo, M.J., 1992. Efficacy of activated sludge in removing Cryptosporidium parvum oocysts from sewage. Appl. Environ. Microbiol. 58, 3514-3516.
57. World Health Organization, 2002. Guidelines for Drinking Water Quality; Addendum - Microbial Agents in Drinking Water, second ed. WHO, Geneva, Switzerland.
58. Xiao, L., Morgan, U.M., Limor, J., Escalante, A., Arrowood, M., Shulaw, W., Thompson, R.C.A., Fayer, R., Lal, A., 1999. Genetic diversity within Cryptosporidium parvum and related Cryptosporidium species. Appl. Environ. Microbiol. 65, 3386-3391.
59. Xiao, L., Fayer, R., Ryan, U., Upton, S.J., 2004. Cryptosporidium taxonomy: recent advances and implications for public health. Clin. Microbiol. Rev. 17, 72-97.
60. Yoder, J., Blackburn, B., Gunther, G., Hill, V., Levy, D., Chen, N., 2004. Surveillance for waterborne-disease outbreaks associated with recreational water - United States, 2001-2002. Washington, DC.
61. Zhou, L., Fayer, R., Trout, J.M., Ryan, U.M., Schaefer III, F.W., Xiao, L., 2004. Genotypes of Cryptosporidium species infecting fur-bearing mammals differ from those of species infecting humans. Appl. Environ. Microbiol. 70, 7574-7577.