Quantitative evaluation of the impact of bather density on levels of human-virulent microsporidian spores in recreational water

Applied and Environmental Microbiology

Volumn 73, Issue 13, 2007, Pages 4095-4099

  Graczyk, Thaddeus K ^a   Sunderland, Deirdre ^a   Tamang, Leena ^a   Shields, Timothy M ^a   Lucy, Frances E ^b   Breysse, Patrick N ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b Atlantic Technological University Sligo   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BATHER DENSITY; MICROSPORIDIAN SPORES; WATERBORNE ETIOLOGY; WATERBORNE SPORES;

CONTAMINATION; EPIDEMIOLOGY; MICROORGANISMS; POTABLE WATER; SEDIMENTS; TURBIDITY; WATER QUALITY;

DISEASES;

EPIDEMIOLOGY; GASTROENTERITIS; IMMUNE SYSTEM; MICROBIAL ACTIVITY; POLLUTION EXPOSURE; PROTOZOAN; RECREATIONAL ACTIVITY; SPORE; VIRULENCE; WATER QUALITY;

ARTICLE; BACTERIUM CONTAMINATION; BATH; ENCEPHALITOZOON INTESTINALIS; ENTEROCYTOZOON; MICROSPORIDIAN SPORE; MICROSPORIDIOSIS; NONHUMAN; PREVALENCE; QUANTITATIVE ANALYSIS; SEDIMENT; TURBIDITY; WATER CONTAMINATION; WATER QUALITY; WATER SAMPLING;

BATHING BEACHES; DNA, FUNGAL; ENCEPHALITOZOON; ENCEPHALITOZOONOSIS; ENTEROCYTOZOON; FRESH WATER; GASTROENTERITIS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MARYLAND; MICROSPORIDIA; MICROSPORIDIOSIS; SPORES, FUNGAL; VIRULENCE; WATER MICROBIOLOGY;

BACTERIA (MICROORGANISMS); ENCEPHALITOZOON INTESTINALIS; ENTEROCYTOZOON BIENEUSI;

EID: 34447543148     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00365-07     Document Type: Article

References (50)

1. Ackerman, D., and S. B. Wisberg. 2003. Relationship between rainfall and beach bacterial concentration on Santa Monica bay beaches. J. Water Health 1:85-89.
2. An, Y. J., D. H. Kampbell, and G. P. Breidenbach. 2002. Escherichia coli and total coliforms in water and sediments at lake marinas. Environ. Pollut. 120:771-778.
3. Ash, L. R., and T. C. Orihel. 1987. Parasites: a guide to laboratory procedures and identification, p. 327. ASCP Press, Chicago, IL.
4. Brookes, J. D., J. Antenucci, M. Hipsey, M. D. Burch, N. J. Ashbolt, and C. Ferguson. 2004. Fate and transport of pathogens in lakes and reservoirs. Environ. Int. 30:741-759.
5. Brusseau, M. L., J. K. Oleen, J. Santamaria, L. Cheng, P. Orosz-Coghlan, A. S. Chetochine, W. J. Blanford, P. Rykwalder, and C. P. Gerba. 2005. Transport of microsporidium Encephalitozoon intestinalis spores in sandy porous media. Water Res. 39:3636-3642.
6. Calderon, R. L., E. W. Mood, and A. P. Dufour. 1991. Health effects of swimming and non-point sources of contaminated water. Int. J. Environ. Health Res. 1:21-31.
7. Cheung, W. H., K. C. Chang, and R. P. Hung. 1991. Variations in microbial indicator densities in beach waters and health-related assessment of bathing water quality. Epidemiol. Infect. 106:329-344.
8. Conteas, C. N., O. G. Berlin, M. J. Lariviere, S. S. Pandhumass, C. E. Speck, R. Porschen, and T. Nakaya. 1998. Examination of the prevalence and seasonal variations of intestinal microsporidiosis in the stools of persons with chronic diarrhea and human immunodeficiency virus infection. Am. J. Trop. Med. Hyg. 58:559-561.
9. Cotte, L., M. Rabodonirina, F. Chapuis, F. Bailly, F. Bissuel, C. Raynal, P. Gelas, F. Persat, M. A. Piens, and C. Treppo. 1999. Waterborne outbreak of intestinal microsporidiosis in persons with and without human immunodeficiency virus infection. J. Infect. Dis. 180:2003-2008.
10. Coupe, S., K. Delabre, R. Pouillot, S. Houdart, M. Santillana-Hayat, and F. Derouin. 2006. Detection of Cryptosporidium, Giardia, and Enterocytozoon bieneusi in surface water, including recreational areas: a one-year prospective study. FEMS Immunol. Med. Microbiol. 47:351-359.
11. Craun, G. F., R. F. Calderon, and M. F. Craun. 2005. Outbreaks associated with recreational water in the United States. Int. J. Environ. Health Res. 15:243-262.
12. Desportes, I., Y. Le Charpentier, A. Galian, F. Bernard, B. Cochand-Priollet, A. Lavergne, P. Ravisse, and R. Modigliani. 1985. Occurrence of a new microsporidian: Enterocytozoon bieneusi n. g., n. sp., in the enterocytes of a human patient with AIDS. J. Protozool. 32:250-254.
13. Didier, E. S., M. E. Stovall, L. C. Green, P. J. Brindley, K. Sestak, and P. J. Didier. 2004. Epidemiology of microsporidiosis: source and modes of transmission. Vet. Parasitol. 126:145-166.
14. Didier, E. S., J. A. Maddry, P. J. Brindley, M. E. Stovall, and P. J. Didier. 2005. Therapeutic strategies for human microsporidia infections. Expert Rev. Anti-Infect. Ther. 3:419-434.
15. Dowd, S. E., C. P. Gerba, and I. L. Pepper. 1998. Confirmation of the human-pathogenic microsporidia Enterocytozoon bieneusi, Encephalitozoon intestinalis, and Vittaforma corneae in water. Appl. Environ. Microbiol. 64: 3332-3335.
16. Dowd, S. E., D. Johns, J. Eliopolus, C. P. Gerba, J. Naranjo, R. Klein, B. Lopez, M. deMejia, C. E. Mendoza, and I. L. Pepper. 2003. Confirmed detection of Cyclospora cayetanensis, Encephalitozoon intestinalis, and Cryptosporidium parvum in water used for drinking. J. Water Health 1:117-123.
17. Elmir, S. M., M. E. Wright, A. Abdelzaher, H. M. Solo-Gabriele, L. E. Fleming, G. Miller, M. Ribolovik, M. P. Shih, S. P. Pillai, J. A. Cooper, and E. A. Quaye. 2007. Quantitative evaluation of bacteria released by bathers in a marine water. Water Res. 41:3-110.
18. Enriquez, F. J., D. Taren, A. Cruz-Lopez, M. Muramoto, J. D. Palting, and P. Cruz. 1998. Prevalence of intestinal encephalitozoonosis in Mexico. Clin. Infect. Dis. 26:1227-1229.
19. Feng, X., D. E. Akiyoshi, A. Sheoran, I. Sigh, J. Hanawald, Q. Zhang, G. Widmer, and S. Tzipori. 2006. Serial propagation of the microsporidian Enterocytozoon bieneusi of human origin in immunocompromised rodents. Infect. Immun. 74:4424-4429.
20. Fleisher, J. M., D. Kay, M. D. Wyer, and A. F. Goodfree. 1989. Estimates of severity of illnesses associated with bathing in marine recreational waters contaminated with domestic sewage. Int. J. Epidemiol. 27:722-726.
21. Fournier, S., O. Liguory, M. Santillana-Hayat, E. Guillot, C. Sarfari, N. Dumoutier, J. Molina, and F. Derouin. 2000. Detection of microsporidia in surface water: a one-year follow-up study. FEMS Immunol. Med. Microbiol. 29:95-100.
22. Franzen, C., and A. Muller. 1999. Cryptosporidia and microsporidia: waterborne diseases in the immunocompromised host. Diagn. Microbiol. Infect. Dis. 34:245-262.
23. Gerba, C. 2000. Assessment of enteric pathogen shedding by bathers during recreational activity and its impact on water quality. Quant. Microbiol. 2:55-68.
24. Gerba, C. P., K. R. Riley, N. Nwachcuku, H. Ryu, and M. Abbaszdegan. 2003. Removal of Encephalitozoon intestinalis, calicivirus, and coliphages by conventional drinking water treatment. J. Environ. Sci. Health 38:1259-1268.
25. Goodgame, R., C. Stager, B. Marcantel, E. Alcocer, and A. M. Segura. 1999. Intensity of infection in AIDS-related intestinal microsporidiosis. J. Infect. Dis. 180:929-932.
26. Graczyk, T. K., and M. R. Cranfield. 2000. Cryptosporidium serpentis oocysts and microsporidian spores in stools of captive snakes. J. Parasitol. 86:413-414.
27. Graczyk, T. K., M. R. Cranfield, and R. Fayer. 1997. Recovery of waterborne oocysts of Cryptosporidium parvum from water samples by the membrane-filter dissolution method. Parasitol. Res. 83:121-125.
28. Graczyk, T. K., D. B. Conn, F. Lucy, D. Minchin, L. Tamang, L. N. S. Moura, and A. J. DaSilva. 2004. Human waterborne parasites in zebra mussels (Dreissena polymorpha) from the Shannon River drainage, Ireland. Parasitol. Res. 93:389-391.
29. Graczyk, T. K., A. S. Girouard, L. Tamang, S. P. Nappier, and K. J. Schwab. 2006. Recovery, bioaccumulation, and inactivation of human waterborne pathogens by the Chesapeake Bay non-native oyster, Crassostrea ariakensis. Appl. Environ. Microbiol. 72:3390-3395.
30. Grimes, D. J. 1975. Release of sediment-bound fecal coliforms by dredging. Appl. Microbiol. 29:109-111.
31. Hanes, N. B., and A. J. Fosa. 1970. A qualitative analysis of the effects of bathers in recreational water quality. Adv. Water Pollut. Res. 5:1-9.
32. Hester, F. D., H. D. A. Linquist, A. M. Bobst, and F. W. Schaffer III. 2000. Fluorescent in situ detection of Encephalitozoon hellem spores with a 6-carboxyfluorescein-labeled ribosomal RNA-targeted oligonucleotide probe. J. Eukaryot. Microbiol. 47:299-308.
33. Jin, G., H. W. Jeng, H. Bradford, and A. J. Englande. 2004. Comparison of E. coli, enterococci, and fecal conform as indicators for brackish water quality assessment. Water Environ. Res. 76:245-255.
34. Kay, D., J. M. Fleisher, R. L. Salmon, F. Jones, M. D. Wyer, A. F. Godfree, Z. Zelenauch-Jacquotte, and R. Shore. 1994. Predicting likelihood of gastroenteritis from sea bathing: results from randomized exposure. Lancet 344:905-909.
35. Mathis, A., R. Weber, and P. Deplazes. 2005. Zoonotic potential of microsporidia. Clin. Microbiol. Rev. 18:423-445.
36. Mota, P., C. A. Rasch, and S. C. Edberg. 2000. Microsporidia and Cyclospora; epidemiology and assessment of the risk from the environment. Crit. Rev. Microbiol. 26:69-90.
37. Mungthin, M., I. Subrungruang, T. Naaglor, P. Aimpun, W. Areekul, and S. Leelayoova. 2005. Spore shedding pattern of Encephalitozoon bieneusi in asymptomatic children. J. Med. Microbiol. 54:473-476.
38. National Resources Defense Council. 2005. Testing the waters 2005. A guide to water quality at vacation beaches. National Resources Defense Council, Washington, DC.
39. Slodkowicz-Kowalska, A., T. K. Graczyk, L. Tamang, S. Jedrzejewski, A. Nowosad, P. Zduniak, P. Solarczyk, A. S. Girouard, and A. C. Majewska. 2006. Microsporidia species known to infect humans are present in aquatic birds: implications for transmission via water? Appl. Environ. Microbiol. 72:4540-4544.
40. Slodkowicz-Kowalska, A., T. K. Graczyk, L. Tamang, A. S. Girouard, and A. Majewska. 2007. Asymptomatic Enterocytozoon bieneusi microsporidiosis in captive mammals. Parasitol. Res. 100:505-509.
41. Sparfel, J. M., C. Sarfati, O. Liquory, B. Caroff, N. Dumoutier, B. Gueglio, E. Billaud, F. Raffi, L. M. Molina, M. Miegeville, and F. Derouin. 1997. Detection of microsporidia and identification of Enterocytozoon bieneusi in surface water by filtration followed by specific PCR. J. Eukaryot. Microbiol. 44:78S.
42. Standish-Lee, and E. Loboschefsky. 2006. Protecting public health from the impact of body contact recreation. Water Sci. Technol. 53:201-207.
43. Steets, B. M., and P. A. Holden. 2003. A mechanistic model of runoff-associated fecal coliform fate and transport through a coastal lagoon. Water Res. 37:589-608.
44. Stewart, M. H., M. V. Yates, M. A. Anderson, C. P. Gerba, J. B. Rose, R. De Leon, and R. L. Wolfe. 2002. Predicted public health consequences of body contact recreation on a potable water reservoir. J. Am. Water Works Assoc. 94:84-97.
45. Thurston-Enriquez, J. A., P. Watt, S. E. Dowd, R. Enriquez, I. L. Pepper, and C. P. Gerba. 2002. Detection of protozoan parasites and microsporidia in irrigation waters used for crop production. J. Food Prot. 65:378-382.
46. U.S. Environmental Protection Agency. 1998. Announcement of the drinking water contaminant candidate list: notice. Fed. Regist. 63:10272-10287.
47. U.S. Environmental Protection Agency. 2002. Implementation criteria for ambient water quality criteria for bacteria. EPA-823-B-02-003. Office of Research and Development, Office of Water, U.S. Environmental Protection Agency, Washington, DC.
48. Wade, T. J., R. L. Calderon, E. Sams, M. Beach, K. P. Brenner, and A. H. Williams. 2006. Rapidly measured indicators of recreational water quality are predictive of swimming-associated gastrointestinal illness. Environ. Health Perspect. 114:24-28.
49. Weber, R., and R. T. Bryan. 1994. Microsporidial infections in immunodeficient and immunocompetent patients. Clin. Infect. Dis. 19:517-521.
50. Zmirou, D., L. Pena, M. Ledrans, and A. Letertre. 2003. Risk associated with microbial quality of bodies of fresh and marine water used for recreational purposes: summary estimates based on published epidemiological studies. Arch. Environ. Health 58:703-711.