Waterborne transmission of Giardia and Cryptosporidium at river beaches in Southern Europe (Portugal)

Journal of Water and Health

Volumn 10, Issue 3, 2012, Pages 484-496

  Júlio, Cláudia ^a   Sá, Cátia ^b   Ferreira, Idalina ^a   Martins, Susana ^a   Oleastro, Mónica ^a   An̂gelo, Helena ^a   Guerreiro, José ^b   Tenreiro, Rogério ^b  

^a NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

Author keywords

Cryptosporidium spp.; Giardia spp.; Portugal; Risk assessment; River beaches; Waterborne transmission

Indexed keywords

BACTERIUM; DISEASE TRANSMISSION; ENVIRONMENTAL INDICATOR; GASTROENTERITIS; HEALTH RISK; PARASITE TRANSMISSION; PATHOGEN; PHYSICOCHEMICAL PROPERTY; POLLUTION EXPOSURE; PROTOZOAN; RECREATIONAL ACTIVITY; RISK ASSESSMENT; RIVER BASIN; SAMPLING; THRESHOLD; WATERBORNE DISEASE;

ARTICLE; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; DISEASE TRANSMISSION; ENTEROCOCCUS; ESCHERICHIA COLI; GIARDIA; GIARDIASIS; INFECTION RISK; NONHUMAN; PHYSICAL CHEMISTRY; PORTUGAL; RIVER; SEASHORE; SEASONAL VARIATION; WATER POLLUTION INDICATOR;

CLUSTER ANALYSIS; CRYPTOSPORIDIUM; GIARDIA; PORTUGAL; PUBLIC HEALTH; RISK FACTORS; RIVERS; WATER MICROBIOLOGY; WATER POLLUTANTS;

PORTUGAL;

CRYPTOSPORIDIUM; ESCHERICHIA COLI; GIARDIA; PROTOZOA;

EID: 84866267982     PISSN: 14778920     EISSN: None     Source Type: Journal    
DOI: 10.2166/wh.2012.030     Document Type: Article

References (54)

1. Almeida, A. A., Delgado, M. L., Soares, S. C., Castro, A. O., Moreira, M. J., Mendonça, C. M., Canada, N. B. & Da Costa, J. M. 2006 Genotype analysis of Giardia isolated from asymptomatic children in northern Portugal. J. Eukaryot. Microbiol. 53 (1), S177-178. (Pubitemid 44813378)
2. Almeida, A., Moreira, M. J., Soares, S., Delgado, M. D. L., Figueiredo, J., Silva, E., Castro, A., Da Costa, A. V. & Correia da Costa, J. M. 2010a Presence of Cryptosporidium spp. and Giardia duodenalis in drinking water samples in the north of Portugal. Korean J. Parasitol. 48 (1), 43- 48.
3. Almeida, A., Moreira, M. J., Soares, S., Delgado, M. L., Figueiredo, J., Magalhães, E. S., Castro, A., Viana Da Costa, A. & Correia da Costa, J. M. 2010b Biological and genetic characterization of Cryptosporidium spp. and Giardia duodenalis isolates from five hydrographical basins in northern Portugal. Korean J. Parasitol. 48 (2), 105-111.
4. Ashbolt, N. J., Grabow, W. O. K. & Snozzi, M. 2001 Indicators of microbial water quality. In: Water Quality: Guidelines, Standards and Health. Assessment of Risk and Risk Management for Water-related Infectious Disease, WHO. IWA Publishing, London, pp. 289-316.
5. Baldursson, S. & Karanis, P. 2011 Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update, 2004-2010. Water Res. 45 (20), 6603-14.
6. 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 (5), 741-759. (Pubitemid 39022754)
7. Brookes, J. D., Hipsey, M. R., Burch, M. D., Regel, R. H., Linden, L. G., Ferguson, C. M. & Antenucci, J. P. 2005 Relative value of surrogate indicators for detecting pathogens in lakes and reservoirs. Environ. Sci. Technol. 39 (22), 8614-8621. (Pubitemid 41636126)
8. Coupe, S., Delabre, K., Pouillot, R., Houdart, S., Santillana-Hayat, M. & Derouin, F. 2006 Detection of Cryptosporidium, Giardia and Enterocytozoon bieneusi in surface water, including recreational areas: a one-year prospective study. FEMS Immunol. Med. Microbiol. 47 (3), 351-359. (Pubitemid 44035885)
9. deRegnier, D. P., Cole, L., Schupp, D. G. & Erlandsen, S. L. 1989 Viability of Giardia cysts suspended in lake, river, and tap water. Appl. Environ. Microbiol. 55 (5), 1223-1229. (Pubitemid 19120720)
10. Directive 2006/7/EC of the European Parliament and of the Council of 15 February 2006 Concerning the management of bathing water quality and repealing Directive 76/160/EEC. Off. J. Eur. Union 4.3.2006, L64/37.
11. Dorner, S. M., Anderson, W. B., Gaulin, T., Candon, H. L., Slawson, R. M., Payment, P. & Huck, P. M. 2007 Pathogen and indicator variability in a heavily impacted watershed. J. Water Health 5 (2), 241- 257.
12. Graczyk, T. K., Sunderland, D., Awantang, G. N., Mashinski, Y., Lucy, F. E., Graczyk, Z., Chomicz, L. & Breysse, P. N. 2010 Relationships among bather density, levels of human waterborne pathogens, and fecal coliform counts in marine recreational beach water. Parasitol. Res. 106 (5), 1103-1108.
13. Groseclose, S. L., Braithwaite, W. L., Hall, P. A., Knowles, C., Adams, D. A., Connor, F., Hester, M., Sharp, P., Anderson, W. J. & Fagan, R. F. 2002 Summary of notifiable diseases - United States 2000. MMWR 49 (53), 1-102.
14. Hansen, J. S.& Ongerth, J. E. 1991 Effects of time and watershed characteristics on the concentration ofCryptosporidiumoocysts in river water. Appl. Environ. Microbiol. 57 (10), 2790-2795.
15. Helmi, K., Skraber, S., Burnet, J. B., Leblanc, L., Hoffmann, L. & Cauchie, H. M. 2011 Two-year monitoring of Cryptosporidium parvum and Giardia lamblia occurrence in a recreational and drinking water reservoir using standard microscopic and molecular biology techniques. Environ. Monit. Assess. 179 (1-4), 163-175.
16. I.M. 2009 Boletim Climatológico Sazonal. Verão 2009, Portugal.
17. I.M. 2010a Boletim Climatológico Sazonal. Inverno 2009/2010, Portugal.
18. I.M. 2010b Boletim Climatológico Sazonal. Verão 2010 Resumo Sazonal, Portugal.
19. Júlio, C., Vilares, A., Oleastro, M., Ferreira, I., Gomes, S., Monteiro, L., Nunes, B., Tenreiro, R. & Ângelo, H. 2012 Prevalence and risk factors for Giardia duodenalis infection among children: a case study in Portugal. Parasit. Vectors 5, 22.
20. Karanis, P., Kourenti, C. & Smith, H. 2007 Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. J. Water Health 5 (1), 1-38. (Pubitemid 46415958)
21. Keeley, A. & Faulkner, B. R. 2008 Influence of land use and watershed characteristics on protozoa contamination in a potential drinking water resources reservoir. Water Res. 42 (10-11), 2803-2813.
22. Kim, L. H., Kayhanian, M., Zoh, K. D. & Stenstrom, M. K. 2005 Modeling of highway stormwater runoff. Sci. Total Environ. 348 (1-3), 1-18. (Pubitemid 41267222)
23. Krometis, L. A., Characklis, G. W., Drummey, P. N. & Sobsey, M. D. 2010 Comparison of the presence and partitioning behavior of indicator organisms and Salmonella spp. in an urban watershed. J. Water Health 8 (1), 44-59.
24. Lane, S. & Lloyd, D. 2002 Current trends in research into the waterborne parasite Giardia. Crit. Rev. Microbiol. 28 (2), 123-147. (Pubitemid 34779348)
25. Lopez, C. E., Juranek, D. D., Sinclair, S. P. & Schultz, M. G. 1978 Giardiasis in American travellers to Madeira Island, Portugal. Am. J. Trop. Med. Hyg. 27 (6), 1128-1132. (Pubitemid 9080429)
26. Mansilha, C. R., Coelho, C. A., Heitor, A. M., Amado, J., Martins, J. P. & Gameiro, P. 2009 Bathing waters: new directive, new standards, new quality approach. Mar. Pollut. Bull. 58 (10), 1562-1565.
27. Matos, O., Tomás, A., Aguiar, P., Casemore, D. & Antunes, F. 1998 Prevalence of Cryptosporidiosis in AIDS patients with diarrhoea in Santa Maria Hospital, Lisbon. Folia Parasitol. (Praha) 45 (2), 163-166. (Pubitemid 28348691)
28. 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 (1), 267-274. (Pubitemid 36077484)
29. Medema, G. J., Schets, F. M., Teunis, P. F. & Havelaar, A. H. 1998 Sedimentation of free and attached Cryptosporidium oocysts and Giardia cysts in water. Appl. Environ. Microbiol. 64 (11), 4460-4466. (Pubitemid 28538018)
30. Melo Cristino, J. A. G., Carvalho, M. I. P. & Salgado, M. J. 1988 An outbreak of cryptosporidiosis in a hospital day-care centre. Epidemiol. Infect. 101, 355-359.
31. Moulin, L., Richard, F., Stefania, S., Goulet, M., Gosselin, S., Gonçalves, A., Rocher, V., Paffoni, C. & Dumètre, A. 2010 Contribution of treated wastewater to the microbiological quality of Seine River in Paris. Water Res. 44 (18), 5222-5231.
32. Nagels, J. W., Davies-Colley, R. J., Donnison, A. M. & Muirhead, R. W. 2002 Faecal contamination over flood events in a pastoral agricultural stream in New Zealand. Water Sci. Technol. 45 (12), 45-52. (Pubitemid 34924975)
33. Nnane, D. E., Ebdon, J. E. & Taylor, H. D. 2011 Integrated analysis of water quality parameters for cost-effective faecal pollution management in river catchments. Water Res. 45 (6), 2235-2246.
34. Noble, R. T., Weisberg, S. B., Leecaster, M. K., McGee, C. D., Dorsey, J. H., Vainik, P. & Orozco-Borbón, V. 2003 Storm effects on regional beach water quality along the southern California shoreline. J. Water Health 1 (1), 23-31.
35. Ottoson, J. & Stenström, T. A. 2003 Faecal contamination of greywater and associated microbial risks. Water Res. 37 (3), 645-655. (Pubitemid 35430327)
36. Plutzer, J., Ongerth, J. & Karanis, P. 2010 Giardia taxonomy, phylogeny and epidemiology: facts and open questions. Int. J. Hyg. Environ. Health 213 (5), 321-333.
37. Robertson, L. J. & Lim, Y. A. L. 2011 Waterborne and environmentally-borne Giardiasis. In: Giardia: A Model Organism (H. D. Luján & S. Svärd, eds.). Springer, Wien, New York, pp. 29-69.
38. Rose, J. B. 1997 Environmental ecology of Cryptosporidium and public health implications. Ann. Rev. Public Health 18, 135-161. (Pubitemid 27194067)
39. Schets, F. M., Engels, G. B. & Evers, E. G. 2004 Cryptosporidium and Giardia in swimming pools in the Netherlands. J. Water Health 2 (3), 191-200.
40. Schets, F. M., Wijnen, J. H., van Schijven, J. F., Schoon, H. & Ronda Husman, A. M. 2008 Monitoring of waterborne pathogens in surface waters in Amsterdam, the Netherlands, and the potential health risk associated with exposure to Cryptosporidium and Giardia in these waters. Appl. Environ. Microbiol. 74 (7), 2069-2078. (Pubitemid 351522060)
41. Schets, F. M., Schijven, J. F. & Roda Husman, A. M. 2011 Exposure assessment for swimmers in bathing waters and swimming pools. Water Res. 45 (7), 2392-2400.
42. Smith, H. & Ahmad, R. 1997 Protozoan parasites in the water. Parasitol. 13 (1), 3- 4.
43. 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. (Pubitemid 47398932)
44. Smith, H. V., Nichols, R. A. B., Connelly, L. & Sullivan, C. B. 2009 Methods for genotyping and subgenotyping Cryptosporidium spp. oocysts isolated during water and food monitoring. In: Giardia and Cryptosporidium: From Molecules to Disease (G. Ortega-Pierres, S. Cacciò, R. Fayer, T. G. Mank, H. V. Smith& R. C. A. Thompson, eds.).CABInternational, UK, pp. 210-226.
45. 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 (15), 3483-3489. (Pubitemid 47031277)
46. Teunis, P. F. M., Medema, G. J., Kruidenier, L. & Havelaar, A. H. 1977 Assessment of the risk of infection by Cryptosporidium or Giardia in drinking water from a surface water source. Water Res. 31 (6), 1333-1346.
47. Thompson, R. C. A., Hopkins, R. M. & Homan, W. L. 2000 Nomenclature and genetic groupings of Giardia infecting mammals early taxonomy. Parasitology 16 (5), 210-213. (Pubitemid 30216567)
48. Tien, J. H. & Earn, D. J. D. 2010 Multiple transmission pathways and disease dynamics in a waterborne pathogen model. Bull. Math. Biol. 72 (6), 1506-1533.
49. Till, D., McBride, G., Ball, A., Taylor, K. & Pyle, E. 2008 Largescale freshwater microbiological study: rationale, results and risks. J. Water Health 6 (4), 443-460.
50. U.S. Environmental Protection Agency (USEPA) 2005 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. U.S. Environmental Protection Agency, Washington, DC, pp. 76.
51. Veldhuis ten, J. A. E., Clemens, F. H. L. R., Sterk, G. & Berends, B. R. 2010 Microbial risks associated with exposure to pathogens in contaminated urban flood water. Water Res. 44, 2910-2918.
52. Vernile, A., Nabi, A. Q., Bonadonna, L., Briancesco, R. & Massa, S. 2009 Occurrence of Giardia and Cryptosporidium in Italian water supplies. Environ. Monit. Assess. 152 (1-4), 203-207.
53. Yoder, J. S. & Beach, M. J. 2010 Cryptosporidium surveillance and risk factors in the United States. Exp. Parasitol. 124 (1), 31-39.
54. World Health Organization 2003 Guidelines for safe recreation water environmental. In: Coastal and Fresh Waters, Vol. 1. World Health Organization, Geneva, pp. 219.