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

California Department of Fish and Game, Marine Wildlife Veterinary Care and Research Center, Santa Cruz, CA 95060, United States.
International Journal for Parasitology (Impact Factor: 3.87). 03/2008; 38(11):1319-28. DOI: 10.1016/j.ijpara.2008.02.005
Source: PubMed


Sea otters in California are commonly infected with Toxoplasma gondii. A unique Type X strain is responsible for 72% of otter infections, but its prevalence in terrestrial animals and marine invertebrates inhabiting the same area was unknown. Between 2000 and 2005, 45 terrestrial carnivores (lions, bobcats, domestic cats and foxes) and 1396 invertebrates (mussels, clams and worms) were screened for T. gondii using PCR and DNA sequencing to determine the phylogeographic distribution of T. gondii archetypal I, II, III and Type X genotypes. Marine bivalves have been shown to concentrate T. gondii oocysts in the laboratory, but a comprehensive survey of wild invertebrates has not been reported. A California mussel from an estuary draining into Monterey Bay was confirmed positive for Type X T. gondii by multilocus PCR and DNA sequencing at the B1 and SAG1 loci. This mussel was collected from nearshore marine waters just after the first significant rainfall event in the fall of 2002. Of 45 carnivores tested at the B1, SAG1, and GRA6 typing loci, 15 had PCR-confirmed T. gondii infection; 11 possessed alleles consistent with infection by archetypal Type I, II or III strains and 4 possessed alleles consistent with Type X T. gondii infection. No non-canonical alleles were identified. The four T. gondii strains with Type X alleles were identified from two mountain lions, a bobcat and a fox residing in coastal watersheds adjacent to sea otter habitat near Monterey Bay and Estero Bay. Confirmation of Type X T. gondii in coastal-dwelling felids, canids, a marine bivalve and nearshore-dwelling sea otters supports the hypotheses that feline faecal contamination is flowing from land to sea through surface runoff, and that otters can be infected with T. gondii via consumption of filter-feeding marine invertebrates.

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    • "The direct agglutination test (DAT; equivalent to the modified agglutination test [MAT]) is a commonly used serologic test for wildlife exposure to T. gondii because it is flexible for use in multiple species (Prestrud et al. 2007), but it has not been formally validated for wildlife and performance can vary among host species (Macrí et al. 2008). Indirect fluorescent antibody tests (IFAT) are also used with wildlife sera (Dabritz et al. 2008; Miller et al. 2008), but their use has been limited to animals for which a taxon-specific secondary antibody has been produced. Both assays have subjective end-point criteria based on visual ins‐ pection, which suggests that the potential exists for misclassification and biased reporting of antibody prevalence. "
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    ABSTRACT: Although the protozoan parasite Toxoplasma gondii is ubiquitous in birds and mammals worldwide, the full suite of hosts and transmission routes is not completely understood, especially in the Arctic. Toxoplasma gondii occurrence in humans and wildlife can be high in Arctic regions, despite apparently limited opportunities for transmission of oocysts shed by felid definitive hosts. Arctic foxes (Vulpes lagopus) are under increasing anthropogenic and ecologic pressure, leading to population declines in parts of their range. Our understanding of T. gondii occurrence in arctic foxes is limited to only a few regions, but mortality events caused by this parasite have been reported. We investigated the exposure of arctic foxes to T. gondii in the Karrak Lake goose colony, Queen Maud Gulf Migratory Bird Sanctuary, Nunavut, Canada. Following an occupancy-modeling framework, we performed replicated antibody analyses on serum samples by direct agglutination test (DAT), indirect fluorescent antibody test (IFAT), and indirect enzyme-linked immunosorbent assay (ELISA) that can be used in multiple mammalian host species. As a metric of test performance, we then estimated the probability of detecting T. gondii antibodies for each of the tests. Occupancy estimates for T. gondii antibodies in arctic foxes under this framework were between 0.430 and 0.758. Detection probability was highest for IFAT (0.716) and lower for DAT (0.611) and ELISA (0.464), indicating that the test of choice for antibody detection in arctic foxes might be the IFAT. We document a new geographic record of T. gondii exposure in arctic foxes and demonstrate an emerging application of ecologic modeling techniques to account for imperfect performance of diagnostic tests in wildlife species.
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    • "In aquatic environments, T. gondii is found in a large variety of marine mammals in California, which is surprising since marine mammals do not consume intermediate hosts. To evaluate how these organisms were infected, Miller et al. (2008) tested tissues collected from various animals along the California coast (terrestrial and marine wildlife and marine and estuarine invertebrates). They found that terrestrial carnivores and wild mussels were infected by the same strain of T. gondii (type X). "

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    • "In the present study using the harbour seal as an animal model for pinnipeds and other closely related marine mammals, we therefore investigated the formation of ETs by PMN and monocytes against the pathogenic apicomplexan protozoa T. gondii. This parasite is a facultative heteroxenous, polyxenous protozoa which possess the capability to infect virtually all warm-blooded animals, including marine mammals (Dubey et al., 2011; Tenter et al., 2000), such as seals (Cabezón et al., 2011; Fujii et al., 2007; Simon et al., 2011), sea otter (Conrad et al., 2005; Goldstein et al., 2011; Miller et al., 2008), dolphins (Dubey et al., 2008) and whales (Mazzariol et al., 2012). To our best knowledge, we here report for the first time on T. gondiitriggered ET formation in harbour seal-PMN and -monocytes. "
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