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Critical processes affecting Cryptosporidium oocyst survival in the environment

Published online by Cambridge University Press:  13 November 2006

B. J. KING  and
P. T. MONIS
B. J. KING
Affiliation:
The Co-operative Research Centre for Water Quality and Treatment, Australian Water Quality Centre, SA Water Corporation, Salisbury, South Australia 5108, Australia
P. T. MONIS
Affiliation:
The Co-operative Research Centre for Water Quality and Treatment, Australian Water Quality Centre, SA Water Corporation, Salisbury, South Australia 5108, Australia
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Abstract

Cryptosporidium are parasitic protozoans that cause gastrointestinal disease and represent a significant risk to public health. Cryptosporidium oocysts are prevalent in surface waters as a result of human, livestock and native animal faecal contamination. The resistance of oocysts to the concentrations of chlorine and monochloramine used to disinfect potable water increases the risk of waterborne transmission via drinking water. In addition to being resistant to commonly used disinfectants, it is thought that oocysts can persist in the environment and be readily mobilized by precipitation events. This paper will review the critical processes involved in the inactivation or removal of oocysts in the terrestrial and aquatic environments and consider how these processes will respond in the context of climate change.

Keywords

Cryptosporidiumsurvivalenvironmentinactivationprocessesreviewclimate change
Type
Review Article
Information
Parasitology , Volume 134 , Issue 3 , March 2007 , pp. 309 - 323
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Alvarez-Pellitero, P. and Sitja-Bobadilla, A. ( 2002). Cryptosporidium molnari n. sp. (Apicomplexa: Cryptosporidiidae) infecting two marine fish species, Sparus aurata L. and Dicentrarchus labrax L. International Journal for Parasitology 32, 1007–1021.Google Scholar
Anderson, B. C., Donndelinger, T., Wilkins, R. M. and Smith, J. ( 1982). Cryptosporidiosis in a Veterinary Student. Journal of the American Veterinary Medical Association 180, 408–409.Google Scholar
Appelbee, A. J., Thompson, R. C. and Olson, M. E. ( 2005). Giardia and Cryptosporidium in mammalian wildlife – current status and future needs. Trends in Parasitology 21, 370–376.CrossRefGoogle Scholar
Arauzo, M. and Valladolid, M. ( 2003). Short-term harmful effects of unionised ammonia on natural populations of Moina micrura and Brachionus rubens in a deep waste treatment pond. Water Research 37, 2547–2554.CrossRefGoogle Scholar
Atwill, E. R., Hoar, B., Das Gracas Cabral Pereira, M., Tate, K. W., Rulofson, F. and Nader, G. ( 2003). Improved quantitative estimates of low environmental loading and sporadic periparturient shedding of Cryptosporidium parvum in adult beef cattle. Applied and Environmental Microbiology 69, 4604–4610.CrossRefGoogle Scholar
Atwill, E. R., Hou, L., Karle, B. M., Harter, T., Tate, K. W. and Dahlgren, R. A. ( 2002). Transport of Cryptosporidium parvum oocysts through vegetated buffer strips and estimated filtration efficiency. Applied and Environmental Microbiology 68, 5517–5527.CrossRefGoogle Scholar
Atwill, E. R., Tate, K. W., Pereira, M. D., Bartolome, J. and Nader, G. ( 2006). Efficacy of natural grassland buffers for removal of Cryptosporidium parvum in rangeland runoff. Journal of Food Protection 69, 177–184.CrossRefGoogle Scholar
Beesley, W. N. ( 1982). The ecological basis of parasite control: ticks and flies. Veterinary Parasitology 11, 99–106.CrossRefGoogle Scholar
Biggane, R. P. J. and Gormally, M. J. ( 1994). The effect of dung beetle activity on the discharge of Pilobolus (Fungi, Mucorales) sporangia in cattle, sheep and horse feces. Entomophaga 39, 95–98.CrossRefGoogle Scholar
Black, E. K., Finch, G. R., Taghi-Kilani, R. and Belosevic, M. ( 1996). Comparison of assays for Cryptosporidium parvum oocysts viability after chemical disinfection. FEMS Microbiology Letters 135, 187–189.CrossRefGoogle Scholar
Brookes, J. D., Antenucci, J., Hipsey, M., Burch, M. D., Ashbolt, N. J. and Ferguson, C. ( 2004). Fate and transport of pathogens in lakes and reservoirs. Environment International 30, 741–759.CrossRefGoogle Scholar
Bukhari, Z., Marshall, M. M., Korich, D. G., Fricker, C. R., Smith, H. V., Rosen, J. and Clancy, J. L. ( 2000). Comparison of Cryptosporidium parvum viability and infectivity assays following ozone treatment of oocysts. Applied and Environmental Microbiology 66, 2972–2980.CrossRefGoogle Scholar
Caccio, S. M. ( 2005). Molecular epidemiology of human cryptosporidiosis. Parassitologia 47, 185–192.Google Scholar
Caldwell, M. M. ( 1971). Solar UV irradiation and the growth and development of higher plants. In Photophysiology, Vol. 6 ( ed. Giese, A. C.), pp. 131–177. Academic Press, NewYork.CrossRef
Causer, L. M., Handzel, T., Welch, P., Carr, M., Culp, D., Lucht, R., Mudahar, K., Robinson, D., Neavear, E., Fenton, S., Rose, C., Craig, L., Arrowood, M., Wahlquist, S., Xiao, L., Lee, Y. M., Mirel, L., Levy, D., Beach, M. J., Poquette, G. and Dworkin, M. S. ( 2006). An outbreak of Cryptosporidium hominis infection at an Illinois recreational waterpark. Epidemiology and Infection 134, 147–156.CrossRefGoogle Scholar
Chauret, C., Nolan, K., Chen, P., Springthorpe, S. and Sattar, S. ( 1998). Aging of Cryptosporidium parvum oocysts in river water and their susceptibility to disinfection by chlorine and monochloramine. Canadian Journal of Microbiology 44, 1154–1160.CrossRefGoogle Scholar
Chen, X. M., O'hara, S. P., Huang, B. Q., Nelson, J. B., Lin, J. J., Zhu, G., Ward, H. D. and Larusso, N. F. ( 2004). Apical organelle discharge by Cryptosporidium parvum is temperature, cytoskeleton, and intracellular calcium dependent and required for host cell invasion. Infection and Immunity 72, 6806–6816.CrossRefGoogle Scholar
Cilimburg, A., Monz, C. and Kehoe, S. ( 2000). PROFILE: Wildland recreation and human waste: a review of problems, practices, and concerns. Environmental Management 25, 587–598.Google Scholar
Clancy, J. L., Marshall, M. M., Hargy, T. M. and Korich, D. G. ( 2004). Susceptibility of five strains of Cryptosporidium parvum oocysts to UV light. Journal of the American Water Works Association 96, 84–93.CrossRefGoogle Scholar
Current, W. L. and Haynes, T. B. ( 1984). Complete development of Cryptosporidium in cell culture. Science 224, 603–605.CrossRefGoogle Scholar
Current, W. L., Reese, N. C., Ernst, J. V., Bailey, W. S., Heyman, M. B. and Weinstein, W. M. ( 1983). Human cryptosporidiosis in immunocompetent and immunodeficient persons. Studies of an outbreak and experimental transmission. The New England Journal of Medicine 308, 1252–1257.CrossRefGoogle Scholar
Dai, X. and Boll, J. ( 2003). Evaluation of attachment of Cryptosporidium parvum and Giardia lamblia to soil particles. Journal of Environmental Quality 32, 296–304.CrossRefGoogle Scholar
Davies, C. M., Altavilla, N., Krogh, M., Ferguson, C. M., Deere, D. A. and Ashbolt, N. J. ( 2005). Environmental inactivation of Cryptosporidium oocysts in catchment soils. Journal of Applied Microbiology 98, 308–317.CrossRefGoogle Scholar
Davies, C. M., Ferguson, C. M., Kaucner, C., Krogh, M., Altavilla, N., Deere, D. A. and Ashbolt, N. J. ( 2004). Dispersion and transport of Cryptosporidium oocysts from fecal pats under simulated rainfall events. Applied and Environmental Microbiology 70, 1151–1159.CrossRefGoogle Scholar
Deckmyn, G. and Impens, I. ( 1999). Seasonal responses of six Poaceae to differential levels of solar UV-B radiation. Environmental and Experimental Botany 41, 177–184.CrossRefGoogle Scholar
Deen, A. and Antenucci, J. P. ( 2000). The Sydney Water contamination incident of 1998-monitoring and modelling. In Hydro 2000, 3rd International Hydrology and Water Resources Symposium, Vol. 1, pp. 103–109. IEAUST, Australia: Institiution of Engineers Australia, Perth, Australia.
Deng, M. Q. and Cliver, D. O. ( 1999). Cryptosporidium parvum studies with dairy products. International Journal of Food Microbiology 46, 113–121.CrossRefGoogle Scholar
Di Giovanni, G. D., Hashemi, F. H., Shaw, N. J., Abrams, F. A., Lechevallier, M. W. and Abbaszadegan, M. ( 1999). Detection of infectious Cryptosporidium parvum oocysts in surface and filter backwash water samples by immunomagnetic separation and integrated cell culture-PCR. Applied and Environmental Microbiology 65, 3427–3432.Google Scholar
Easterling, D. R., Meehl, G. A., Parmesan, C., Changnon, S. A., Karl, T. R. and Mearns, L. O. ( 2000). Climate extremes: observations, modeling, and impacts. Science 289, 2068–2074.CrossRefGoogle Scholar
Fayer, R. ( 1994). Effect of high temperature on infectivity of Cryptosporidium parvum oocysts in water. Applied and Environmental Microbiology 60, 2732–2735.Google Scholar
Fayer, R., Dubey, J. P. and Lindsay, D. S. ( 2004). Zoonotic protozoa: from land to sea. Trends in Parasitology 20, 531–536.CrossRefGoogle Scholar
Fayer, R., Graczyk, T. K., Cranfield, M. R. and Trout, J. M. ( 1996). Gaseous disinfection of Cryptosporidium parvum oocysts. Applied and Environmental Microbiology 62, 3908–3909.Google Scholar
Fayer, R., Graczyk, T. K., Lewis, E. J., Trout, J. M. and Farley, C. A. ( 1998 a). Survival of infectious Cryptosporidium parvum oocysts in seawater and eastern oysters (Crassostrea virginica) in the Chesapeake Bay. Applied and Environmental Microbiology 64, 1070–1074.Google Scholar
Fayer, R., Morgan, U. and Upton, S. J ( 2000 a). Epidemiology of Cryptosporidium: transmission, detection and identification. International Journal for Parasitology 30, 1305–1322.Google Scholar
Fayer, R. and Nerad, T. ( 1996). Effects of low temperatures on viability of Cryptosporidium parvum oocysts. Applied and Environmental Microbiology 62, 1431–1433.Google Scholar
Fayer, R., Trout, J. M. and Jenkins, M. C. ( 1998 b). Infectivity of Cryptosporidium parvum oocysts stored in water at environmental temperatures. Journal of Parasitology 84, 1165–1169.Google Scholar
Fayer, R., Trout, J. M., Lewis, E. J., Xiao, L., Lal, A., Jenkins, M. C. and Graczyk, T. K. ( 2002). Temporal variability of Cryptosporidium in the Chesapeake Bay. Parasitology Research 88, 998–1003.Google Scholar
Fayer, R., Trout, J. M., Walsh, E. and Cole, R. ( 2000 b). Rotifers ingest oocysts of Cryptosporidium parvum. Journal of Eukaryotic Microbiology 47, 161–163.Google Scholar
Ferguson, C., Husman, A. M. D., Altavilla, N., Deere, D. and Ashbolt, N. ( 2003). Fate and transport of surface water pathogens in watersheds. Critical Reviews in Environmental Science and Technology 33, 299–361.CrossRefGoogle Scholar
Fincher, G. T. ( 1975). Effects of dung beetle activity on the number of nematode parasites acquired by grazing cattle. Journal of Parasitology 61, 759–762.CrossRefGoogle Scholar
Follet-Dumoulin, A., Guyot, K., Duchatelle, S., Bourel, B., Guilbert, F., Dei-Cas, E., Gosset, D. and Cailliez, J. C. ( 2001). Involvement of insects in the dissemination of Cryptosporidium in the environment. Journal of Eukaryotic Microbiology (Suppl.) 36S.CrossRefGoogle Scholar
Freire-Santos, F., Oteiza-Lopez, A. M., Castro-Hermida, J. A., Garcia-Martin, O. and Ares-Mazas, M. E. ( 2001). Viability and infectivity of oocysts recovered from clams, Ruditapes philippinarum, experimentally contaminated with Cryptosporidium parvum. Parasitology Research 87, 428–430.Google Scholar
Freire-Santos, F., Oteiza-Lopez, A. M., Vergara-Castiblanco, C. A. and Ares-Mazas, E. ( 2000 a). Study of the combined influence of environmental factors on viability of Cryptosporidium parvum oocysts in water evaluated by fluorogenic vital dyes and excystation techniques. Veterinary Parasitology 89, 253–259.Google Scholar
Freire-Santos, F., Oteiza-Lopez, A. M., Vergara-Castiblanco, C. A., Ares-Mazas, E., Alvarez-Suarez, E. and Garcia-Martin, O. ( 2000 b). Detection of Cryptosporidium oocysts in bivalve molluscs destined for human consumption. Journal of Parasitology 86, 853–854.Google Scholar
Freire-Santos, F., Oteiza-Lopez, A. M., Vergara-Castiblanco, C. A. and Ares-Mazas, M. E. ( 1999). Effect of salinity, temperature and storage time on mouse experimental infection by Cryptosporidium parvum. Veterinary Parasitology 87, 1–7.CrossRefGoogle Scholar
Friedberg, E., Walker, G. and Siede, W. ( 1995). DNA and Mutagenesis. ASM Press, Washington, DC.
Fuller, W. H. and Warrick, A. ( 1985). Soils in Waste Treatment and Utilization. Vol. I ( ed. Press, C.), pp. 268. Boca Raton, FL.
Giangaspero, A., Molini, U., Iorio, R., Traversa, D., Paoletti, B. and Giansante, C. ( 2005). Cryptosporidium parvum oocysts in seawater clams (Chameleagallina) in Italy. Preventative Veterinary Medicine 69, 203–212.CrossRefGoogle Scholar
Gomez-Couso, H., Freire-Santos, F., Amar, C. F., Grant, K. A., Williamson, K., Ares-Mazas, M. E. and McLauchlin, J. ( 2004). Detection of Cryptosporidium and Giardia in molluscan shellfish by multiplexed nested-PCR. International Journal of Food Microbiology 91, 279–288.CrossRefGoogle Scholar
Gomez-Couso, H., Freire-Santos, F., Martinez-Urtaza, J., Garcia-Martin, O. and Ares-Mazas, M. E. ( 2003). Contamination of bivalve molluscs by Cryptosporidium oocysts: the need for new quality control standards. International Journal of Food Microbiology 87, 97–105.CrossRefGoogle Scholar
Graczyk, T. K., Fayer, R., Knight, R., Mhangami-Ruwende, B., Trout, J. M., Da Silva, A. J. and Pieniazek, N. J. ( 2000). Mechanical transport and transmission of Cryptosporidium parvum oocysts by wild filth flies. American Journal of Tropical Medicine and Hygiene 63, 178–183.CrossRefGoogle Scholar
Graczyk, T. K., Knight, R. and Tamang, L. ( 2005). Mechanical transmission of human protozoan parasites by insects. Clinical Microbiological Reviews 18, 128–132.CrossRefGoogle Scholar
Hader, D. P., Kumar, H. D., Smith, R. C. and Worrest, R. C. ( 1998). Effects on aquatic ecosystems. Journal of Photochemistry and Photobiology B-Biology 46, 53–68.CrossRefGoogle Scholar
Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S. and Samuel, M. D. ( 2002). Ecology – climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.CrossRefGoogle Scholar
Harvey, K. ( 2004). Investigation into the predation of Cryptosporidium in the environment. Thesis, Health Sciences, University of South Australia, Adelaide.
Hawkins, P. R., Swanson, P., Warnecke, M., Shanker, S. R. and Nicholson, C. ( 2000). Understanding the fate of Cryptosporidium and Giardia in storage reservoirs: a legacy of Sydney's water contamination incident. Journal of Water Supply Research and Technology-Aqua 49, 289–306.CrossRefGoogle Scholar
Hijjawi, N. S., Meloni, B. P., Morgan, U. M. and Thompson, R. C. ( 2001). Complete development and long-term maintenance of Cryptosporidium parvum human and cattle genotypes in cell culture. International Journal for Parasitology 31, 1048–1055.CrossRefGoogle Scholar
Hijnen, W. A. M., Beerendonk, E. F. and Medema, G. J. ( 2006). Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. Water Research 40, 3–22.CrossRefGoogle Scholar
Hollosy, F. ( 2002). Effects of ultraviolet radiation on plant cells. Micron 33, 179–197.CrossRefGoogle Scholar
Huamanchay, O., Genzlinger, L., Iglesias, M. and Ortega, Y. R. ( 2004). Ingestion of Cryptosporidium oocysts by Caenorhabditis elegans. Journal of Parasitology 90, 1176–1178.CrossRefGoogle Scholar
Hughes-Hanks, J. M., Rickard, L. G., Panuska, C., Saucier, J. R., O'hara, T. M., Dehn, L. and Rolland, R. M. ( 2005). Prevalence of Cryptosporidium spp. and Giardia spp. in five marine mammal species. Journal of Parasitology 91, 1225–1228.Google Scholar
Hughes, K. A., Lawley, B. and Newsham, K. K. ( 2003). Solar UV-B radiation inhibits the growth of Antarctic terrestrial fungi. Applied and Environmental Microbiology 69, 1488–1491.CrossRefGoogle Scholar
Hunter, P., Syed, Q. and Naumova, E. N. ( 2001). Possible undetected outbreaks of cryptosporidiosis in areas of the north west of England supplied by an unfiltered surface water source. Communicable Disease and Public Health 4, 136–138.Google Scholar
Hunter, P. R. and Thompson, R. C. ( 2005). The zoonotic transmission of Giardia and Cryptosporidium. International Journal for Parasitology 35, 1181–1190.CrossRefGoogle Scholar
Hutchison, M. L., Walters, L. D., Moore, T., Thomas, D. J. and Avery, S. M. ( 2005). Fate of pathogens present in livestock wastes spread onto fescue plots. Applied and Environmental Microbiology 71, 691–696.CrossRefGoogle Scholar
IASC ( 1995). Effects of increased ultraviolet radiation in the Artic. IASC Report No. 2, IASC Secretariat, Journal of Plant Physiology 148, 42–48.
Jenkins, M. B., Bowman, D. D., Fogarty, E. A. and Ghiorse, W. C. ( 2002). Cryptosporidium parvum oocyst inactivation in three soil types at various temperatures and water potentials. Soil Biology and Biochemistry 34, 1101–1109.CrossRefGoogle Scholar
Jenkins, M. B., Bowman, D. D. and Ghiorse, W. C. ( 1998). Inactivation of Cryptosporidium parvum oocysts by ammonia. Applied and Environmental Microbiology 64, 784–788.Google Scholar
Jenkins, M. B., Bowman, D. D. and Ghiorse, W. C. ( 1999 a). Inactivation of Cryptosporidium parvum oocysts by ammonia (vol 64, pg 784, 1998). Applied and Environmental Microbiology 65, 1362.Google Scholar
Jenkins, M. B., Walker, M. J., Bowman, D. D., Anthony, L. C. and Ghiorse, W. C. ( 1999 b). Use of a sentinel system for field measurements of Cryptosporidium parvum oocyst inactivation in soil and animal waste. Applied and Environmental Microbiology 65, 1998–2005.Google Scholar
Jenkins, M. C., Trout, J., Abrahamsen, M. S., Lancto, C. A., Higgins, J. and Fayer, R. ( 2000). Estimating viability of Cryptosporidium parvum oocysts using reverse transcriptase-polymerase chain reaction (RT-PCR) directed at mRNA encoding amyloglucosidase. Journal of Microbiological Methods 43, 97–106.CrossRefGoogle Scholar
Jerome, J. H. and Bukata, R. P. ( 1998). Tracking the propagation of solar ultraviolet radiation: dispersal of ultraviolet photons in inland waters. Journal of Great Lakes Research 24, 666–680.CrossRefGoogle Scholar
Johnson, A. M., Linden, K., Ciociola, K. M., De Leon, R., Widmer, G. and Rochelle, P. A. ( 2005). UV inactivation of Cryptosporidium hominis as measured in cell culture. Applied and Environmental Microbiology 71, 2800–2802.CrossRefGoogle Scholar
Johnson, D. C., Enriquez, C. E., Pepper, I. L., Davis, T. L., Gerba, C. P. and Rose, J. B. ( 1997). Survival of Giardia, Cryptosporidium, poliovirus and Salmonella in marine waters. Water Science and Technology 35, 261–268.CrossRefGoogle Scholar
Juranek, D. D. ( 1997). Cryptosporidium and water: a public health handbook – 1997. Clinical Laboratory Science 10, 272.Google Scholar
Kato, S., Jenkins, M., Fogarty, E. and Bowman, D. ( 2004). Cryptosporidium parvum oocyst inactivation in field soil and its relation to soil characteristics: analyses using the geographic information systems. Science of the Total Environment 321, 47–58.CrossRefGoogle Scholar
Kato, S., Jenkins, M. B., Fogarty, E. A. and Bowman, D. D. ( 2002). Effects of freeze-thaw events on the viability of Cryptosporidium parvum oocysts in soil. Journal of Parasitology 88, 718–722.Google Scholar
Keegan, A. R., Fanok, S., Monis, P. T. and Saint, C. P. ( 2003). Cell culture-Taqman PCR assay for evaluation of Cryptosporidium parvum disinfection. Applied and Environmental Microbiology 69, 2505–2511.CrossRefGoogle Scholar
Khramtsov, N. V. and Upton, S. J. ( 1998). High-temperature inducible cell-free transcription and replication of double-stranded RNAs within the parasitic protozoan Cryptosporidium parvum. Virology 245, 331–337.CrossRefGoogle Scholar
Khramtsov, N. V. and Upton, S. J. ( 2000). Association of RNA polymerase complexes of the parasitic protozoan Cryptosporidium parvum with virus-like particles: heterogeneous system. Journal of Virology 74, 5788–5795.CrossRefGoogle Scholar
King, B. J., Keegan, A. R., Monis, P. T. and Saint, C. P. ( 2005). Environmental temperature controls Cryptosporidium oocyst metabolic rate and associated retention of infectivity. Applied and Environmental Microbiology 71, 3848–3857.CrossRefGoogle Scholar
LeChevallier, M. W., Norton, W. D., Siegel, J. E. and Abbaszadegan, M. ( 1995). Evaluation of the immunofluorescence procedure for detection of Giardia cysts and Cryptosporidium oocysts in water. Applied and Environmental Microbiology 61, 690–697.Google Scholar
Li, X., Atwill, E. R., Dunbar, L. A., Jones, T., Hook, J. and Tate, K. W. ( 2005). Seasonal temperature fluctuations induces rapid inactivation of Cryptosporidium parvum. Environmental Science and Technology 39, 4484–4489.CrossRefGoogle Scholar
Mackenzie, W. R., Schell, W. L., Blair, K. A., Addiss, D. G., Peterson, D. E., Hoxie, N. J., Kazmierczak, J. J. and Davis, J. P. ( 1995). Massive outbreak of waterborne Cryptosporidium infection in Milwaukee, Wisconsin: recurrence of illness and risk of secondary transmission. Clinical Infectious Diseases 21, 57–62.CrossRefGoogle Scholar
MacRae, M., Hamilton, C., Strachan, N. J., Wright, S. and Ogden, I. D. ( 2005). The detection of Cryptosporidium parvum and Escherichia coli O157 in UK bivalve shellfish. Journal of Microbiological Methods 60, 395–401.CrossRefGoogle Scholar
Malloy, K. D., Holman, M. A., Mitchell, D. and Detrich, H. W., 3rd ( 1997). Solar UVB-induced DNA damage and photoenzymatic DNA repair in antarctic zooplankton. Proceedings of the National Academy of Sciences, USA 94, 1258–1263.CrossRefGoogle Scholar
Mathison, B. A. and Ditrich, O. ( 1999). The fate of Cryptosporidium parvum oocysts ingested by dung beetles and their possible role in the dissemination of cryptosporidiosis. Journal of Parasitology 85, 678–681.CrossRefGoogle Scholar
Mawdsley, J. L., Bardgett, R. D., Merry, R. J., Pain, B. F. and Theodorou, M. K. ( 1995). Pathogens in livestock waste, their potential for movement through soil and environmental pollution. Applied Soil Ecology 2, 1–15.CrossRefGoogle Scholar
Mawdsley, J. L., Brooks, A. E. and Merry, R. J. ( 1996). Movement of the protozoan pathogen Cryptosporidium parvum through three contrasting soil types. Biology and Fertility of Soils 21, 30–36.CrossRefGoogle Scholar
McGechan, M. B. ( 2002). Transport of particulate and colloid-sorbed contaminants through soil, part 2: trapping processes and soil pore geometry. Biosystems Engineering 83, 387–395.CrossRefGoogle Scholar
Medema, G. J., Schets, F. M., Teunis, P. F. and Havelaar, A. H. ( 1998). Sedimentation of free and attached Cryptosporidium oocysts and Giardia cysts in water. Applied and Environmental Microbiology 64, 4460–4466.Google Scholar
Meisel, J. L., Perera, D. R., Meligro, C. and Rubin, C. E. ( 1976). Overwhelming watery diarrhea associated with a Cryptosporidium in an immunosuppressed patient. Gastroenterology 70, 1156–1160.Google Scholar
Messner, M. J., Chappell, C. L. and Okhuysen, P. C. ( 2001). Risk assessment for Cryptosporidium: a hierarchical Bayesian analysis of human dose response data. Water Research 35, 3934–3940.CrossRefGoogle Scholar
Michallet, H. and Ivey, G. N. ( 1999). Experiments on mixing due to internal solitary waves breaking on uniform slopes. Journal of Geophysical Research – Oceans 104, 13467–13477.CrossRefGoogle Scholar
Misra, R. B., Lal, K., Farooq, M. and Hans, R. K. ( 2005). Effect of solar UV radiation on earthworm (Metaphire posthuma). Ecotoxicology and Environmental Safety 62, 391–396.CrossRefGoogle Scholar
Monis, P. T. and Thompson, R. C. ( 2003). Cryptosporidium and Giardia-zoonoses: fact or fiction? Infection, Genetics and Evolution 3, 233–244.Google Scholar
Moriarty, E. M., Duffy, G., Mcevoy, J. M., Caccio, S., Sheridan, J. J., Mcdowell, D. and Blair, I. S. ( 2005). The effect of thermal treatments on the viability and infectivity of Cryptosporidium parvum on beef surfaces. Journal of Applied Microbiology 98, 618–623.CrossRefGoogle Scholar
Morris, D. P., Zagarese, H., Williamson, C. E., Balseiro, E. G., Hargreaves, B. R., Modenutti, B., Moeller, R. and Queimalinos, C. ( 1995). The attentuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnology and Oceanography 40, 1381–1391.CrossRefGoogle Scholar
Muck, R. E. and Richards, B. K. ( 1983). Losses of manurial nitrogen in free-stall barns. Agricultural Wastes 7, 65–79.CrossRefGoogle Scholar
Muck, R. E. and Steenhuis, T. S. ( 1982). Nitrogen losses from manure storages. Agricultural Wastes 4, 41–54.CrossRefGoogle Scholar
Naganuma, T., Konishi, S., Inoue, T., Nakane, T. and Sukizaki, S. ( 1996). Photodegradation or photoalteration? Microbial assay of the effect of UV-B on dissolved organic matter. Marine Ecology Progress Series 135, 309–310.CrossRefGoogle Scholar
Nasser, A. M., Teuto, E., Tenenbaum, L. and Netzan, Y. ( 2003). Die-off of Cryptosporidium spp. in tap water, in seawater and in soil: comparision between infectivity and viability. In IWA Health Related Water Microbiology Symposium, London. IWA, Cape Town, Africa.
O'Donoghue, P. J. ( 1995). Cryptosporidium and cryptosporidiosis in man and animals. International Journal for Parasitology 25, 139–195.CrossRefGoogle Scholar
Ongerth, J. E. and Pecoraro, J. P. ( 1996). Electrophoretic mobility of Cryptosporidium oocysts and Giardia cysts. Journal of Environmental Engineering-Asce 122, 228–231.CrossRefGoogle Scholar
Overpeck, J. T., Otto-Bliesner, B. L., Miller, G. H., Muhs, D. R., Alley, R. B. and Kiehl, J. T. ( 2006). Paleoclimatic evidence for future ice-sheet instability and rapid sea-level rise. Science 311, 1747–1750.CrossRefGoogle Scholar
Patni, N. K. and Jui, P. Y. ( 1991). Nitrogen concentration variability in dairy-cattle slurry stored in farm tanks. Transactions of the Asae 34, 609–615.CrossRefGoogle Scholar
Patterson, J. L. ( 1993). The current status of Leishmania RNA virus I. Parasitology Today 9, 135–136.CrossRefGoogle Scholar
Pereira, S. J., Ramirez, N. E., Xiao, L. and Ward, L. A. ( 2002). Pathogenesis of human and bovine Cryptosporidium parvum in gnotobiotic pigs. Journal of Infectious Diseases 186, 715–718.CrossRefGoogle Scholar
Piazena, H. and Hader, D. P. ( 1994). Penetration of solar UV irradiation in coastal lagoons of the southern Baltic Sea and its effect on phytoplankton communities. Photochemistry and Photobiology 60, 463–469.CrossRefGoogle Scholar
Power, M. L., Shanker, S. R., Sangster, N. C. and Veal, D. A. ( 2003). Evaluation of a combined immunomagnetic separation/flow cytometry technique for epidemiological investigations of Cryptosporidium in domestic and Australian native animals. Veterinary Parasitology 112, 21–31.CrossRefGoogle Scholar
Ravanat, J. L., Douki, T. and Cadet, J. ( 2001). Direct and indirect effects of UV radiation on DNA and its components. Journal of Photochemistry and Photobiology B-Biology 63, 88–102.CrossRefGoogle Scholar
Reese, N. C., Current, W. L., Ernst, J. V. and Bailey, W. S. ( 1982). Cryptosporidiosis of man and calf: a case report and results of experimental infections in mice and rats. American Journal of Tropical Medicine and Hygiene 31, 226–229.CrossRefGoogle Scholar
Reynolds, C. S. ( 1984). The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge, UK.
Ries, G., Heller, W., Puchta, H., Sandermann, H., Seidlitz, H. K. and Hohn, B. ( 2000). Elevated UV-B radiation reduces genome stability in plants. Nature 406, 98–101.CrossRefGoogle Scholar
Robertson, L. J., Campbell, A. T. and Smith, H. V. ( 1992). Survival of Cryptosporidium parvum oocysts under various environmental pressures. Applied and Environmental Microbiology 58, 3494–3500.Google Scholar
Robertson, L. J. and Gjerde, B. K. ( 2004). Effects of the Norwegian winter environment on Giardia cysts and Cryptosporidium oocysts. Microbial Ecology 47, 359–365.CrossRefGoogle Scholar
Rochelle, P. A., Ferguson, D. M., Handojo, T. J., De Leon, R., Stewart, M. H. and Wolfe, R. L. ( 1997). An assay combining cell culture with reverse transcriptase PCR to detect and determine the infectivity of waterborne Cryptosporidium parvum. Applied and Environmental Microbiology 63, 2029–2037.Google Scholar
Rochelle, P. A., Marshall, M. M., Mead, J. R., Johnson, A. M., Korich, D. G., Rosen, J. S. and De Leon, R. ( 2002). Comparison of in vitro cell culture and a mouse assay for measuring infectivity of Cryptosporidium parvum. Applied and Environmental Microbiology 68, 3809–3817.CrossRefGoogle Scholar
Rochelle, P. A., Upton, S. J., Montelone, B. A. and Woods, K. ( 2005). The response of Cryptosporidium parvum to UV light. Trends in Parasitology 21, 81–87.CrossRefGoogle Scholar
Rossignol, J. F., Kabil, S. M., El-Gohary, Y. and Younis, A. M. ( 2006). Effect of nitazoxanide in diarrhea and enteritis caused by Cryptosporidium species. Clinical Gastroenterology and Hepatology 4, 320–324.CrossRefGoogle Scholar
Ruxton, G. D. ( 1995). Mathematical-modeling of ammonia volatilization from slurry stores and its effect on Cryptosporidium oocyst viability. Journal of Agricultural Science 124, 55–60.Google Scholar
Shin, G. A., Linden, K. G., Arrowood, M. J. and Sobsey, M. D. ( 2001). Low-pressure UV inactivation and DNA repair potential of Cryptosporidium parvum oocysts. Applied and Environmental Microbiology 67, 3029–3032.CrossRefGoogle Scholar
Sitja-Bobadilla, A., Padros, F., Aguilera, C. and Alvarez-Pellitero, P. ( 2005). Epidemiology of Cryptosporidium molnari in Spanish gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.) cultures: from hatchery to market size. Applied and Environmental Microbiology 71, 131–139.Google Scholar
Slieman, T. A. and Nicholson, W. L. ( 2000). Artificial and solar UV radiation induces strand breaks and cyclobutane pyrimidine dimers in Bacillus subtilis spore DNA. Applied and Environmental Microbiology 66, 199–205.CrossRefGoogle Scholar
Slifko, T. R., Friedman, D., Rose, J. B. and Jakubowski, W. ( 1997). An in vitro method for detecting infectious Cryptosporidium oocysts with cell culture. Applied and Environmental Microbiology 63, 3669–3675.Google Scholar
Slifko, T. R., Huffman, D. E., Dussert, B., Owens, J. H., Jakubowski, W., Haas, C. N. and Rose, J. B. ( 2002). Comparison of tissue culture and animal models for assessment of Cryptospridium parvum infection. Experimental Parasitology 101, 97–106.CrossRefGoogle Scholar
Smith, H. V. and Corcoran, G. D. ( 2004). New drugs and treatment for cryptosporidiosis. Current Opinion in Infectious Diseases 17, 557–564.CrossRefGoogle Scholar
Smith, H. V. and Rose, J. B. ( 1990). Waterborne cryptosporidiosis. Parasitology Today 6, 8–12.CrossRefGoogle Scholar
Smith, H. V. and Rose, J. B. ( 1998). Waterborne cryptosporidiosis: current status. Parasitology Today 14, 14–22.CrossRefGoogle Scholar
SoloGabriele, H. and Neumeister, S. ( 1996). US outbreaks of cryptosporidiosis. Journal American Water Works Association 88, 76–86.CrossRefGoogle Scholar
Sreter, T. and Varga, I. ( 2000). Cryptosporidiosis in birds – a review. Veterinary Parasitology 87, 261–279.CrossRefGoogle Scholar
Stott, R., May, E., Matsushita, E. and Warren, A. ( 2001). Protozoan predation as a mechanism for the removal of Cryptosporidium oocysts from wastewaters in constructed wetlands. Water Science and Technology 44, 191–198.CrossRefGoogle Scholar
Stott, R., May, E., Ramirez, E. and Warren, A. ( 2003). Predation of Cryptosporidium oocysts by protozoa and rotifers: implications for water quality and public health. Water Science and Technology 47, 77–83.CrossRefGoogle Scholar
Sturdee, A. P., Chalmers, R. M. and Bull, S. A. ( 1999). Detection of Cryptosporidium oocysts in wild mammals of mainland Britain. Veterinary Parasitology 80, 273–280.CrossRefGoogle Scholar
Szostakowska, B., Kruminis-Lozowska, W., Racewicz, M., Knight, R., Tamang, L., Myjak, P. and Graczyk, T. K. ( 2004). Cryptosporidium parvum and Giardia lamblia recovered from flies on a cattle farm and in a landfill. Applied and Environmental Microbiology 70, 3742–3744.CrossRefGoogle Scholar
Tai, J. H., Chang, S. C., Chou, C. F. and Ong, S. J. ( 1996). Separation and characterization of two related giardiaviruses in the parasitic protozoan Giardia lamblia. Virology 216, 124–132.CrossRefGoogle Scholar
Tate, K. W., Pereira, M. D. and Atwill, E. R. ( 2004). Efficacy of vegetated buffer strips for retaining Cryptosporidium parvum. Journal of Environmental Quality 33, 2243–2251.CrossRefGoogle Scholar
Theodos, C. M., Griffiths, J. K., D'onfro, J., Fairfield, A. and Tzipori, S. ( 1998). Efficacy of nitazoxanide against Cryptosporidium parvum in cell culture and in animal models. Antimicrobial Agents and Chemotherapy 42, 1959–1965.Google Scholar
Thomas, D. M., Stanton, N. L. and Seville, R. S. ( 1995). A stable Eimerian assemblage in Wyoming ground squirrels (Spermophilus elegans elegans) – maintaining viability over winter. Journal of the Helminthological Society of Washington 62, 1–5.Google Scholar
Tillett, H. E., De Louvois, J. and Wall, P. G. ( 1998). Surveillance of outbreaks of waterborne infectious disease: categorizing levels of evidence. Epidemiology and Infection 120, 37–42.CrossRefGoogle Scholar
Trask, J. R., Kalita, P. K., Kuhlenschmidt, M. S., Smith, R. D. and Funk, T. L. ( 2004). Overland and near-surface transport of Cryptosporidium parvum from vegetated and nonvegetated surfaces. Journal of Environmental Quality 33, 984–993.CrossRefGoogle Scholar
Upton, S. J., Tilley, M., Nesterenko, M. V. and Brillhart, D. B. ( 1994). A simple and reliable method of producing in vitro Infections of Cryptosporidium parvum (Apicomplexa). FEMS Microbiology Letters 118, 45–49.CrossRefGoogle Scholar
Wadhams, P. and Munk, W. ( 2004). Ocean freshening, sea level rising, sea ice melting. Geophysical Research Letters 31, Article no. L11311, June 12.CrossRefGoogle Scholar
Walker, M., Leddy, K. and Hager, E. ( 2001). Effects of combined water potential and temperature stresses on Cryptosporidium parvum oocysts. Applied and Environmental Microbiology 67, 5526–5529.CrossRefGoogle Scholar
Wang, A. L. and Wang, C. C. ( 1986). Discovery of a specific double-stranded RNA virus in Giardia lamblia. Molecular and Biochemical Parasitology 21, 269–276.CrossRefGoogle Scholar
Wang, A. L. and Wang, C. C. ( 1991). Viruses of parasitic protozoa. Parasitology Today 7, 76–80.CrossRefGoogle Scholar
Whitehead, D. C. and Raistrick, N. ( 1993). The volatilization of ammonia from cattle urine applied to soils as influenced by soil properties. Plant and Soil 148, 43–51.CrossRefGoogle Scholar
Whitman, R. L., Nevers, M. B., Korinek, G. C. and Byappanahalli, M. N. ( 2004). Solar and temporal effects on Escherichia coli concentration at a Lake Michigan swimming beach. Applied and Environmental Microbiology 70, 4276–4285.CrossRefGoogle Scholar
Widmer, G., Orbacz, E. A. and Tzipori, S. ( 1999). beta-tubulin mRNA as a marker of Cryptosporidium parvum oocyst viability. Applied and Environmental Microbiology 65, 1584–1588.Google Scholar
Xiao, L., Ryan, U. M., Graczyk, T. K., Limor, J., Li, L., Kombert, M., Junge, R., Sulaiman, I. M., Zhou, L., Arrowood, M. J., Koudela, B., Modry, D. and Lal, A. A. ( 2004). Genetic diversity of Cryptosporidium spp. in captive reptiles. Applied and Environmental Microbiology 70, 891–899.CrossRefGoogle Scholar
Zyman, J. and Sorber, C. A. ( 1988). Influence of simulated rainfall on the transport and survival of selected indicator organisms in sludge-amended soils. Journal of the Water Pollution Control Federation 60, 2105–2110.Google Scholar