Fate and transport of Toxoplasma gondii oocysts in seasonally snow covered watersheds: A conceptual framework from a melting snowpack to the canadian arctic coasts

International Journal of Environmental Research and Public Health

Volumn 10, Issue 3, 2013, Pages 995-1005

  Simon, Audrey ^a   Poulin, Michel Bigras ^a   Rousseau, Alain N ^b   Ogden, Nicholas H ^a,c  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CENTRE EAU TERRE ENVIRONNEMENT   (Canada)

^c PUBLIC HEALTH AGENCY OF CANADA   (Canada)

Author keywords

Estuary; Faeces borne pathogen; Hydrological transport; Large scale dispersion; Snowmelt runoff; Toxoplasma gondii; Waterborne contamination

Indexed keywords

SURFACE WATER; SNOW;

COASTAL ZONE; CONCEPTUAL FRAMEWORK; ENVIRONMENTAL FATE; ESTUARINE POLLUTION; MARINE POLLUTION; MELTING; PATHOGEN; POLLUTANT TRANSPORT; PROTOZOAN; RUNOFF; SNOW COVER; SNOWMELT; SNOWPACK; WATERSHED;

ARCTIC; ARTICLE; CANADA; CONCEPTUAL FRAMEWORK; DEFECATION; ENVIRONMENTAL IMPACT; FOOD POISONING; GEOGRAPHIC DISTRIBUTION; HABITAT USE; HOST PARASITE INTERACTION; HUMAN; INFECTION RISK; MARINE ENVIRONMENT; NONHUMAN; OOCYST; PARASITE INCIDENCE; PARASITE LOAD; PARASITE SURVIVAL; PARASITE VIABILITY; SEASONAL VARIATION; SEDIMENTATION; SOIL POLLUTION; SPOROGENESIS; STREAM (RIVER); TEMPERATURE SENSITIVITY; TOXOPLASMOSIS; ULTRAVIOLET RADIATION; WATER CONTAMINATION; WATERSHED; ANIMAL; REVIEW; SEASON; SOIL POLLUTANT; TOXOPLASMA; WATER FLOW; WATER POLLUTANT; WATER SUPPLY;

CANADA; CANADIAN ARCTIC;

ANIMALS; ARCTIC REGIONS; CANADA; OOCYSTS; SEASONS; SNOW; SOIL POLLUTANTS; TOXOPLASMA; WATER MOVEMENTS; WATER POLLUTANTS; WATER SUPPLY;

MLCS; MLOWN;

EID: 84875267417     PISSN: 16617827     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph10030994     Document Type: Article

References (48)

1. Ferguson, C.; Husman, A.M.D.; Altavilla, N.; Deere, D.; Ashbolt, N. Fate and transport of surface water pathogens in watersheds. Crit. Rev. Environ. Sci. Tech. 2003, 33, 299-361.
2. Thomas, M.K.; Charron, D.F.; Waltner-Toews, D.; Schuster, C.; Maarouf, A.R.; Holt, J.D. A role of high impact weather events in waterborne disease outbreaks in Canada, 1975-2001. Int. J. Environ. Health Rev. 2006, 16, 167-180.
3. Baldursson, S.; Karanis, P. Waterborne transmission of protozoan parasites: Review of worldwide outbreaks-An update 2004-2010. Water Res. 2011, 45, 6603-6614.
4. Bowie, W.R.; King, A.S.; Werker, D.H.; Isaac-Renton, J.L.; Bell, A.; Eng, S.B.; Marion, S.A. Outbreak of toxoplasmosis associated with municipal drinking water. The BC Toxoplasma investigation team. Lancet 1997, 350, 173-177.
5. Whitman, R.L.; Przybyla-Kelly, K.; Shively, D.A.; Nevers, M.B.; Byappanahalli, M.N. Sunlight, season, snowmelt, storm, and source affect E. coli populations in an artificially ponded stream. Sci. Total Environ. 2008, 390, 448-455.
6. Zhu, Z.X.; Broersma, K.; Mazumder, A. Model assessment of cattle and climate impacts on stream fecal coliform pollution in the salmon river watershed, British Columbia, Canada. Water Air Soil Pollut. 2011, 215, 155-176.
7. Meyer, T.; Wania, F. Organic contaminant amplification during snowmelt. Water Res. 2008, 42, 1847-1865.
8. Simon, A.; Chambellant, M.; Ward, B.J.; Simard, M.; Proulx, J.F.; Levesque, B.; Bigras-Poulin, M.; Rousseau, A.N.; Ogden, N.H. Spatio-temporal variations and age effect on Toxoplasma gondii seroprevalence in seals from the Canadian Arctic. Parasitology 2011, 138, 1362-1368.
9. Dubey, J.P. Toxoplasmosis of Animals and Humans, 2nd ed.; CRC Press: Boca Raton, FL, USA, 2010.
10. Cole, R.A.; Lindsay, D.S.; Howe, D.K.; Roderick, C.L.; Dubey, J.P.; Thomas, N.J.; Baeten, L.A. Biological and molecular characterizations of Toxoplasma gondii strains obtained from southern sea otters (Enhydra lutris nereis). J. Parasitol. 2000, 86, 526-530.
11. Conrad, P.A.; Miller, M.A.; Kreuder, C.; James, E.R.; Mazet, J.; Dabritz, H.; Jessup, D.A.; Gulland, F.; Grigg, M.E. Transmission of Toxoplasma: Clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. Int. J. Parasitol. 2005, 35, 1155-1168.
12. Miller, M.A.; Gardner, I.A.; Kreuder, C.; Paradies, D.M.; Worcester, K.R.; Jessup, D.A.; Dodd, E.; Harris, M.D.; Ames, J.A.; Packham, A.E.; et al. Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis). Int. J. Parasitol. 2002, 32, 997-1006.
13. Miller, M.A.; Miller, W.A.; Conrad, P.A.; James, E.R.; Melli, A.C.; Leutenegger, C.M.; Dabritz, H.A.; Packham, A.E.; Paradies, D.; et al. Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: New linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters. Int. J. Parasitol. 2008, 38, 1319-1328.
14. Vanwormer, E.; Fritz, H.; Shapiro, K.; Mazet, J.A.; Conrad, P.A. Molecules to modeling: Toxoplasma gondii oocysts at the human-animal-environment interface. Comp. Immunol Microbiol. Infect. Dis. 2012, doi: 10.1016/j.cimid.2012.1010.1006.
15. Simon, A.; Poulin, M.B.; Rousseau, A.N.; Dubey, J.P.; Ogden, N.H. Spatiotemporal dynamics of Toxoplasma gondii infection in Canadian lynx (Lynx canadensis) in Western Quebec, Canada. J. Wildlife Dis. 2013, 49, 39-48.
16. Jokelainen, P.; Isomursu, M.; Nareaho, A.; Oksanen, A. Natural Toxoplasma gondii infections in european brown hares and mountain hares in Finland: Proportional mortality rate, antibody prevalence, and genetic characterization. J. Wildlife Dis. 2011, 47, 154-163.
17. Frenkel, J.K.; Dubey, J.P. Effects of freezing on the viability of Toxoplasma oocysts. J. Parasitol. 1973, 59, 587-588.
18. Yilmaz, S.M.; Hopkins, S.H. Effects of different conditions on duration of infectivity of Toxoplasma gondii oocysts. J. Parasitol. 1972, 58, 938-939.
19. Woo, M.-K. Northern hydrology. In Canada's Cold Environments; French, H.M., Slaymaker, O., Eds. McGill-Queen's University Press: Montréal, Canada, 1993; pp. 117-142.
20. Mann, M.E.; Schmidt, G.A. Ground vs. surface air temperature trends: Implications for borehole surface temperature reconstructions. Geophys. Res. Lett. 2003, 30, doi: 10.1029/2003GL017170
21. Lindsay, D.S.; Blagburn, B.L.; Dubey, J.P. Survival of nonsporulated Toxoplasma gondii oocysts under refrigerator conditions. Vet. Parasitol. 2002, 103, 309-313.
22. Mowat, G.; Poole, K.G.; O'Donoghue, M. Ecology of lynx in northern Canada and Alaska. In Ecology and Conservation of Lynx in the United States; Ruggerio, L.F., Aubry, K.B., Buskirk, S.W., Koehler, G.M., Krebs, C.J., McKelvey, K.S.; Squires, J.R., Eds.; University of Colorado Press: Boulder, Co, USA, 2000; pp. 265-306.
23. Dubey, J.P. Toxoplasma gondii oocyst survival under defined temperatures. J. Parasitol 1998, 84, 862-865.
24. Frenkel, J.K.; Ruiz, A.; Chinchilla, M. Soil survival of Toxoplasma oocysts in Kansas and Costa Rica. Am. J. Trop Med. Hyg. 1975, 24, 439-443.
25. Lelu, M.; Villena, I.; Darde, M.L.; Aubert, D.; Geers, R.; Dupuis, E.; Marnef, F.; Poulle, M.L.; Gotteland, C.; Dumetre, A.; et al. Quantitative estimation of the viability of Toxoplasma gondii oocysts in soil. Appl. Environ. Microbol. 2012, 78, 5127-5132.
26. Shapiro, K.; Largier, J.; Mazet, J.A.; Bernt, W.; Ell, J.R.; Melli, A.C.; Conrad, P.A. Surface properties of Toxoplasma gondii oocysts and surrogate microspheres. Appl. Environ. Microbiol. 2009, 75, 1185-1191.
27. Jamieson, R.; Gordon, R.; Joy, D.; Lee, H. Assessing microbial pollution of rural surface waters-A review of current watershed scale modeling approaches. Agr. Water Manag. 2004, 70, 1-17.
28. Davies, C.M.; Ferguson, C.M.; Kaucner, C.; Krogh, M.; Altavilla, N.; Deere, D.A.; Ashbolt, N.J. Dispersion and transport of Cryptosporidium oocysts from fecal pats under simulated rainfall events. Appl. Environ. Microbol. 2004, 70, 1151-1159.
29. McGechan, M.B.; Lewis, D.R. Transport of particulate and colloid-sorbed contaminants through soil, part 1: General principles. Biosyst. Eng. 2002, 83, 255-273.
30. Fraser, R.H.; Barten, P.K.; Pinney, D.A.K. Predicting stream pathogen loading from livestock using a geographical information system-based delivery model. J. Environ. Qual. 1998, 27, 935-945.
31. Tate, K.W.; Pereira, M.D.; Atwill, E.R. Efficacy of vegetated buffer strips for retaining Cryptosporidium parvum. J. Environ. Qual. 2004, 33, 2243-2251.
32. Dumetre, A.; Aubert, D.; Puech, P.H.; Hohweyer, J.; Azas, N.; Villena, I. Interaction forces drive the environmental transmission of pathogenic protozoa. Appl. Environ. Microbol. 2012, 78, 905-912.
33. Shapiro, K.; Conrad, P.A.; Mazet, J.A.; Wallender, W.W.; Miller, W.A.; Largier, J.L. Effect of estuarine wetland degradation on the transport of Toxoplasma gondii surrogates from land to sea. Appl. Environ. Microbiol. 2010, 76, 6821-6828.
34. Mann, K.H.; Lazier, J.R.N. Dynamics of Marine Ecosystems Biological-Physical Interactions in the Oceans, 3rd ed.; Blackwell Pub.: Malden, MA, USA, 2006.
35. Shapiro, K.; Silver, M.W.; Largier, J.L.; Conrad, P.A.; Mazet, J.A.K. Association of Toxoplasma gondii oocysts with fresh, estuarine, and marine macroaggregates. Limnol. Oceanogr. 2012, 57, 449-456.
36. Lindsay, D.S.; Collins, M.V.; Mitchell, S.M.; Cole, R.A.; Flick, G.J.; Wetch, C.N.; Lindquist, A.; Dubey, J.P. Sporulation and survival of Toxoplasma gondii oocysts in seawater. J. Eukaryot. Microbiol. 2003, 50, 687-688.
37. Lindsay, D.S.; Dubey, J.P. Long-term survival of Toxoplasma gondii sporulated oocysts in seawater. J. Parasitol. 2009, 95, 1019-1020.
38. Johnson, C.K.; Tinker, M.T.; Estes, J.A.; Conrad, P.A.; Staedler, M.; Miller, M.A.; Jessup, D.A.; Mazet, J.A. Prey choice and habitat use drive sea otter pathogen exposure in a resource-limited coastal system. Proc. Natl. Acad. Sci. USA 2009, 106, 2242-2247.
39. Jones, J.L.; Dargelas, V.; Roberts, J.; Press, C.; Remington, J.S.; Montoya, J.G. Risk factors for Toxoplasma gondii infection in the United States. Clin. Infect. Dis. 2009, 49, 878-884.
40. Arkush, K.D.; Miller, M.A.; Leutenegger, C.M.; Gardner, I.A.; Packham, A.E.; Heckeroth, A.R.; Tenter, A.M.; Barr, B.C.; Conrad, P.A. Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis). Int. J. Parasitol. 2003, 33, 1087-1097.
41. Lindsay, D.S.; Phelps, K.K.; Smith, S.A.; Flick, G.; Sumner, S.S.; Dubey, J.P. Removal of Toxoplasma gondii oocysts from sea water by eastern oysters (Crassostrea virginica). J. Eukaryot. Microbiol. 2001, 48, 197S-198S.
42. Lindsay, D.S.; Collins, M.V.; Mitchell, S.M.; Wetch, C.N.; Rosypal, A.C.; Flick, G.J.; Zajac, A.M.; Lindquist, A.; Dubey, J.P. Survival of Toxoplasma gondii oocysts in Eastern oysters (Crassostrea virginica). J. Parasitol. 2004, 90, 1054-1057.
43. Fayer, R.; Dubey, J.P.; Lindsay, D.S. Zoonotic protozoa: From land to sea. Trends Parasitol. 2004, 20, 531-536.
44. Massie, G.N.; Ware, M.W.; Villegas, E.N.; Black, M.W. Uptake and transmission of Toxoplasma gondii oocysts by migratory, filter-feeding fish. Vet. Parasitol. 2010, 169, 296-303.
45. Dubey, J.P.; Lunney, J.K.; Shen, S.K.; Kwok, O.C.H.; Ashford, D.A.; Thulliez, P. Infectivity of low numbers of Toxoplasma gondii oocysts to pigs. J. Parasitol. 1996, 82, 438-443.
46. Dubey, J.P.; Speer, C.A.; Shen, S.K.; Kwok, O.C.H.; Blixt, J.A. Oocyst-induced murine toxoplasmosis: Life cycle, pathogenicity, and stage conversion in mice fed Toxoplasma gondii oocysts. J. Parasitol. 1997, 83, 870-882.
47. Karanis, P.; Aldeyarbi, H.M.; Mirhashemi, M.E.; Khalil, K.M. The impact of the waterborne transmission of Toxoplasma gondii and analysis efforts for water detection: An overview and update. Environ. Sci. Pollut. Res. Int. 2013, 20, 86-99.
48. Ferguson, C.M.; Charles, K.; Deere, D.A. Quantification of microbial sources in drinking-water catchments. Crit. Rev. Envron. Sci. Tech. 2009, 39, 1-40.