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

International Journal for Parasitology

Volumn 38, Issue 11, 2008, Pages 1319-1328

  Miller, M A ^a   Miller, W A ^b   Conrad, P A ^b   James, E R ^c   Melli, A C ^b   Leutenegger, C M ^d   Dabritz, H A ^e   Packham, A E ^b   Paradies, D ^f   Harris, M ^a   Ames, J ^a   Jessup, D A ^a   Worcester, K ^g   Grigg, M E ^h  

^a CALIFORNIA DEPARTMENT OF FISH AND GAME   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d IDEXX LABORATORIES   (United States)

^e Infant Botulism Treatment and Prevention Program   (United States)

^f Bay Foundation of Morro Bay   (United States)

^g Central Coast Regional Water Quality Control Board   (United States)

^h NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

18S rDNA; B1; Felid; GRA6; Mussel; Otter; SAG1; Toxoplasma gondii; Type X

Indexed keywords

PROTOZOAL DNA; RUNOFF; SEA WATER;

BIVALVE; CARNIVORE; FECES; FELID; MAMMAL; MUSTELID; PARASITE PREVALENCE; PROTOZOAN; WILD POPULATION;

ALLELE; ANIMAL PARASITOSIS; ARTICLE; CANONICAL ANALYSIS; CARNIVORA; CARNIVORE; CAT; CLAM; DNA SEQUENCE; DOMESTIC ANIMAL; FECES; FOX; GENE IDENTIFICATION; INVERTEBRATE; LINKAGE ANALYSIS; LION; MUSSEL; NONHUMAN; OOCYST; POLYMERASE CHAIN REACTION; SEASHORE; TERRESTRIAL SPECIES; TOXOPLASMA GONDII; UNITED STATES; WORM;

ANIMALS; BIVALVIA; CALIFORNIA; DNA, PROTOZOAN; ENVIRONMENTAL MONITORING; FECES; FELIDAE; OCEANS AND SEAS; OOCYSTS; OTTERS; POLYMERASE CHAIN REACTION; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL;

CALIFORNIA; MONTEREY BAY; NORTH AMERICA; UNITED STATES;

ANIMALIA; BIVALVIA; CANIDAE; ENHYDRA; FELIDAE; FELIS CATUS; INVERTEBRATA; LUTRINAE; LYNX RUFUS; MAMMALIA; MYTILUS CALIFORNIANUS; PUMA CONCOLOR; TOXOPLASMA GONDII;

EID: 48549088611     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2008.02.005     Document Type: Article

References (55)

1. Ajzenberg D., Bañuls A.L., Su C., Dumetre A., Demar M., Carme B., and Dardé M.L. Genetic diversity, clonality and sexuality in Toxoplasma gondii. Int. J. Parasitol. 34 (2004) 1185-1196
2. Aramini J.J., Stephen C., Dubey J.P., Engelstoft C., Schwantje H., and Ribble C.S. Potential contamination of drinking water with Toxoplasma gondii oocysts. Epidemiol. Infect. 122 (1999) 305-315
3. Arkush K.D., Miller M.A., Leutenegger C.M., Gardner I.A., Packham A.E., Heckeroth A.R., Tenter A.M., Barr B.C., and Conrad P.A. Molecular and bioassay-detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis). Int. J. Parasitol. 33 (2003) 1087-1097
4. Bahia-Oliveira L.M., Jone G., Azevedo-Silva L.M., Alves C.C.F., Orefice F., and Addiss D.G. Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro state, Brazil. Emerg. Infect. Dis. 9 (2003) 55-62
5. Benenson M.W., Takafuji E.T., Lemon S.M., Greenup R.L., and Sulzer A.J. Oocyst-transmitted toxoplasmosis associated with ingestion of contaminated water. N. Engl. J. Med. 307 (1982) 666-669
6. Bowie W.R., King A.S., Walker D.H., Isaac-Renton J.L., Bell A., Eng S.B., and Marion S.A. Outbreak of toxoplasmosis associated with municipal drinking water. Lancet 350 (1997) 173-177
7. Burg J.L., Grover C.M., Pouletty P., and Boothroyd J.C. Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain reaction. J. Clin. Microbiol. 27 (1989) 1787-1792
8. Conrad P.A., Miller M.A., Kreuder C., James E.R., Mazet J., Dabritz H., Jessup D., Gulland F., and Grigg M. Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. Int. J. Parasitol. 35 (2005) 1155-1168
9. Dabritz H.A., Atwill E.R., Gardner I.A., Miller M.A., and Conrad P.A. Outdoor fecal deposition by free-roaming cats and attitudes of cat owners and nonowners toward stray pets, wildlife, and water pollution. J. Am. Vet. Med. Assoc. 229 (2006) 74-81
10. Dabritz H.A., Miller M.A., Atwill E.R., Gardner I.A., Leutenegger C.M., Melli A.C., and Conrad P.A. Detection of Toxoplasma gondii-like oocysts in cat feces and estimates of the environmental oocyst burden. J. Am. Vet. Med. Assoc. 231 (2007) 1676-1684
11. Dardé M.L. Biodiversity in Toxoplasma gondii. Curr. Top. Microbiol. Immunol. 219 (1996) 27-41
12. Dawson D. Foodborne protozoal parasites. Int. J. Food Microbiol. 103 (2005) 207-227
13. de Moura L., Bahia-Oliveira L.M., Wada M.Y., Jones J.L., Tuboi S.H., Carmo E.H., Ramalho W.M., Camargo N.J., Trevisan R., Graca R.M., da Silva A.J., Moura I., Dubey J.P., and Garrett D.O. Waterborne toxoplasmosis, Brazil, from field to gene. Emerg. Infect. Dis. 12 (2006) 326-329
14. Delmas P., and Regis M.B. Preliminary findings on the contents of the edible urchin Paracentrotus lividus (Lamarck) when subjected to the influence of domestic effluents [Donnés preliminaries sur le contenu digestif de l'oursin comestible Paracentrotus lividus (Lamarck) soumis à l'influence d'effluents domestiques]. Mar. Environ. Res. 20 (1986) 197-220
15. Dubey J.P. Toxoplasma, Neospora, Sarcocystis and other tissue cyst-forming coccidia of humans and animals. In: Krier J.P. (Ed). Parasitic Protozoa. second ed. vol. 6 (1993), Academic Press, Inc., San Diego, CA 158
16. Dubey J.P., and Beattie C.P. Toxoplasmosis of Animals and Man (1988), CRC Press, Boca Raton, Florida (pp. 220)
17. Dubey J.P., Lunney J.K., Shen S.K., Kwok O.C., Ashford D.A., and Thulliez P. Infectivity of low numbers of Toxoplasma gondii oocysts to pigs. J. Parasitol. 82 (1996) 438-443
18. Dubey J.P., Speer C.A., Shen S.K., Kwok O.C., and Blixt J.A. Oocyst-induced murine toxoplasmosis: life cycle, pathogenicity, and stage conversion in mice fed Toxoplasma gondii oocysts. J. Parasitol. 83 (1997) 870-882
19. Dubey J.P., Storandt S.T., Kwok O.C.H., Thulliez P., and Kazacos K.R. Toxoplasma gondii antibodies in naturally exposed wild coyotes, red foxes, and gray foxes and serologic diagnosis of toxoplasmosis in red foxes fed T. gondii oocysts and tissue cysts. J. Parasitol. 85 (1999) 240-243
20. Dubey J.P., Graham D.H., Dahl E., Streekmar C., Lehman T., Davis M.F., and Morishita T.Y. Toxoplasma gondii isolates from free-ranging chickens from the United States. J. Parasitol. 89 (2003) 1060-1062
21. Dubey J.P., Zarnke R.L., Thomas N.J., Wong S.K., Van Bonn W., Briggs M., Davis J.W., Ewing R., Mense M., Kwok O.C., Romand S., and Thulliez P. Toxoplasma gondii, Neospora caninum, Sarcocystis neurona, and Sarcocystis canis-like infections in marine mammals. Vet. Parasitol. 116 (2003) 275-296
22. Dubey J.P., Salant H., Streekmar C., Dhal E., Vianna M.C., Shen S.K., Kwok O.C., Spira D., Hamburger J., and Lehmann T.V. High prevalence of Toxoplasma gondii in a commercial flock of chickens in Israel, and public health implications of free-range farming. Vet. Parasitol. 121 (2004) 317-322
23. Dubey J.P., Graham D.H., De Young R.W., Dahl E., Eberhard M.L., Nace E.K., Won K., Bishop H., Punksody G., Streekmar C., Vianna M.C., Shen S.K., Kwok O.C., Summers J.A., Demarais S., Hill D.E., Chirukandoth S., and Dubey J.P. Biology and epidemiology of Toxoplasma gondii in man and animals. Anim. Health Res. Rev. 6 (2005) 41-61
24. Enriquez R., Frösner G.G., Hochstein-Mintzel V., Riedemann S., and Reinhardt G. Accumulation and persistence of hepatitis A virus in mussels. J. Med. Virol. 37 (1992) 174-179
25. Fayer R., Dubey J.P., and Lindsay D.S. Zoonotic protozoa: from land to sea. Trends Parasitol. 20 (2004) 531-536
26. Ferreira A.M., Vitor R.W., Carneiro A.C., Brandao G.P., and Melo M.N. Genetic variability of Brazilian Toxoplasma gondii strains detected by random amplified polymorphic DNA-polymerase chain reaction (RAPD-PCR) and simple sequence repeat anchored PCR (SSR-PCR). Infect. Genet. Evol. 4 (2004) 131-142
27. Grigg M.E., and Boothroyd J.C. Rapid identification of virulent Type I strains of the protozoan pathogen Toxoplasma gondii by PCR-restriction fragment length polymorphism analysis at the B1 gene. J. Clin. Microbiol. 39 (2001) 398-400
28. Grigg M.E., and Suzuki Y. Sexual recombination and clonal evolution of virulence in Toxoplasma. Microbes and Infect. 5 (2003) 685-690
29. Grigg M.E., Bonnefoy S., Hehl A.B., Suzuki Y., and Boothroyd J.C. Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries. Science 294 (2001) 161-165
30. Grigg M.E., Ganatra J., Boothroyd J.C., and Margolis T.P. Unusual abundance of atypical strains associated with human ocular toxoplasmosis. J. Infect. Dis. 184 (2001) 633
31. Howe D.K., and Sibley L.D. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J. Infect. Dis. 172 (1995) 1561-1566
32. Kreuder C., Miller M.A., Jessup D.A., Lowenstine L.J., Harris M.D., Ames J.A., Carpenter T.E., Conrad P.A., and Mazet J.A. Recent patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998-2001. J. Wildl. Dis. 39 (2003) 495-509
33. Lefebvre K.A., Powell C.L., Busman M., Doucette G.J., Moeller P.D., Silver J.B., Hughes M.P., Singaram S., Silver M.W., and Tjeerdema R.S. Detection of domoic acid in northern anchovies and California sea lions associated with an unusual mortality event. Nat. Toxins 7 (1999) 85-92
34. Lindsay D.S., Phelps K.K., Smith S.A., Flick G., and Dubey J.P. Removal of Toxoplasma gondii oocysts from seawater by eastern oysters (Crassostrea virginica). J. Eukaryot. Microbiol. (2001) 197S-198S
35. Lindsay D.S., Collins M.V., Mitchell S.M., Welch C.N., Rosypal A.C., Flick G.J., Zajac A.M., Lindquist A., and Dubey J.P. Survival of Toxoplasma gondii oocysts in eastern oysters (Crassostrea virginica). J. Parasitol. 90 (2004) 1054-1057
36. Mallin M.A., Williams K.E., Esham E.C., and Lowe R.P. Effect of human development on bacteriological water quality in coastal watersheds. Ecol. Appl. 10 (2000) 1047-1056
37. Miller, M.A., 2008. Tissue cyst-forming coccidia of marine mammals. In: Fowler, M., Miller, E. (Eds.), Zoo and Wild Animal Medicine, Current Therapy, sixth ed., W.B. Saunders Press. Philadelphia, PA, pp. 319-340.
38. Miller M.A., Sverlow K.W., Crosbie P.R., Barr B.C., Lowenstine L.J., Gulland F.M., Packham A., and Conrad P.A. Isolation and characterization of two parasitic protozoa from a pacific harbor seal (Phoca vitulina richardsi) with meningoencephalomyelitis. J. Parasitol. 87 (2001) 816-822
39. Miller M.A., Gardner I.A., Packham A., Mazet J.K., Hanni K.D., Jessup D.A., Estes J., Jameson R., Dodd E., Barr B.C., Lowenstine L.J., Gulland F.M., and Conrad P.A. Evaluation of an indirect fluorescent antibody test (IFAT) for demonstration of antibodies to Toxoplasma gondii in the sea otter (Enhydra lutris). J. Parasitol. 88 (2002) 594-599
40. 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., and Conrad P.A. Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis). Int. J. Parasitol. 32 (2002) 997-1006
41. Miller M.A., Grigg M.E., Kreuder C., James E.R., Melli A.C., Crosbie P.R., Jessup D.A., Boothroyd J.C., Brownstein D., and Conrad P.A. An unusual genotype of Toxoplasma gondii is common in California sea otters (Enhydra lutris nereis) and is a cause of mortality. Int. J. Parasitol. 34 (2004) 275-284
42. Miller W.A., Atwill E.R., Gardner I.A., Miller M.A., Fritz H.M., Hedrick R.P., Melli A.C., Barnes N.M., and Conrad P.A. Clams (Corbicula fluminea) as bioindicators of fecal contamination with Cryptosporidium and Giardia spp. in freshwater ecosystems of California. Int. J. Parasitol. 35 (2005) 673-684
43. Miller W.A., Miller M.A., Gardner I.A., Atwill E.R., Harris M.D., Ames J.A., Jessup D.A., Melli A.C., Paradies D., Worcester K., Olin P., Barnes N., and Conrad P.A. New genotypes and factors associated with Cryptosporidium detection in mussels, (Mytilus spp.) along the California coast. Int. J. Parasitol. 35 (2005) 1103-1113
44. Miller W.A., Gardner I.A., Leutenegger C.M., Miller M.A., Atwill E.R., Hedrick R.P., Melli A.C., Barnes N.M., and Conrad P.A. Evaluation of methods for improved detection of Cryptosporidium spp. in mussels (Mytilus californianus). J. Microbiol. Methods 65 (2006) 367-379
45. Miller W.A., Miller M.A., Gardner I.A., Atwill R.E., Byrne B., Jang S.S., Harris M., Ames J., Jessup D.A., Paradies D., Worcester K., Melli A.C., and Conrad P.A. Salmonella spp., Vibrio spp., Clostridium perfringens, and Plesiomonas shigelloides in marine and freshwater invertebrates from coastal California ecosystems. Microb. Ecol. 52 (2006) 198-206
46. Osovitz C.J., and Julian D. Burrow irrigation behavior of Urechis caupo, a filter-feeding marine invertebrate, in its natural habitat. Mar. Ecol.-Prog. Ser. 245 (2002) 149-155
47. Palanisamy M., Madhavan B., Balasundaram M.B., Andavar R., and Venkatapathy N. Outbreak of ocular toxoplasmosis in Coimbatore, India. Indian J. Opthalmol. 54 (2006) 129-131
48. Pereira M.D.G., Atwill E.R., and Jones T. Comparison of sensitivity of immunofluorescent microscopy to that of a combination of immunofluorescent microscopy and immunomagnetic separation for detection of Cryptosporidium parvum in adult bovine feces. Appl. Environ. Microbiol. 65 (1999) 3226-3239
49. Roper D.S., and Hickey C.W. Effects of food and silt on filtration, respiration and condition of the freshwater mussel Hyridella menziesi (Unionacea: Hyriidae): Implications for bioaccumulation. Hydrobiologia 312 (1995) 17-25
50. Ruiz A., and Frenkel J.K. Toxoplasma gondii in Costa Rican cats. Am. J. Trop. Med. Hyg. 2 (1980) 1150-1160
51. Su C., Evans D., Cole R., Kissinger J., Ajioka J., and Sibley L. Recent Expansion of Toxoplasma through enhanced oral transmission. Science 299 (2003) 414-416
52. Su C., Zhang X., and Dubey J.P. Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. Int. J. Parasitol. 36 (2006) 841-848
53. Tenter A.M., Heckeroth A.R., and Weiss L.M. Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30 (2000) 1217-1258
54. Thompson R.C., Olsen Y., Mitchell R.P., Davis A., Rowland S.J., John A.W., McGonigle D., and Russell A.E. Lost at sea: where is all the plastic?. Science 304 (2004) 838
55. Young K.D., and Thackston E.L. Housing density and bacterial loading in urban streams. J. Environ. Eng. 125 (1999) 1177-1180