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      Polyparasitism Is Associated with Increased Disease Severity in Toxoplasma gondii-Infected Marine Sentinel Species

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          Abstract

          In 1995, one of the largest outbreaks of human toxoplasmosis occurred in the Pacific Northwest region of North America. Genetic typing identified a novel Toxoplasma gondii strain linked to the outbreak, in which a wide spectrum of human disease was observed. For this globally-distributed, water-borne zoonosis, strain type is one variable influencing disease, but the inability of strain type to consistently explain variations in disease severity suggests that parasite genotype alone does not determine the outcome of infection. We investigated polyparasitism (infection with multiple parasite species) as a modulator of disease severity by examining the association of concomitant infection of T. gondii and the related parasite Sarcocystis neurona with protozoal disease in wild marine mammals from the Pacific Northwest. These hosts ostensibly serve as sentinels for the detection of terrestrial parasites implicated in water-borne epidemics of humans and wildlife in this endemic region. Marine mammals (151 stranded and 10 healthy individuals) sampled over 6 years were assessed for protozoal infection using multi-locus PCR-DNA sequencing directly from host tissues. Genetic analyses uncovered a high prevalence and diversity of protozoa, with 147/161 (91%) of our sampled population infected. From 2004 to 2009, the relative frequency of S. neurona infections increased dramatically, surpassing that of T. gondii. The majority of T. gondii infections were by genotypes bearing Type I lineage alleles, though strain genotype was not associated with disease severity. Significantly, polyparasitism with S. neurona and T. gondii was common (42%) and was associated with higher mortality and more severe protozoal encephalitis. Our finding of widespread polyparasitism among marine mammals indicates pervasive contamination of waterways by zoonotic agents. Furthermore, the significant association of concomitant infection with mortality and protozoal encephalitis identifies polyparasitism as an important factor contributing to disease severity in marine mammals.

          Author Summary

          Severity of toxoplasmosis, a water-borne zoonosis, varies widely from chronic and benign to acutely fatal. Here, we investigate polyparasitism (infection with multiple parasite species) as one factor governing the spectrum of disease in Toxoplasma gondii infections. This study utilized wild marine mammals as sentinels to detect contamination of waterways by T. gondii and a similar protozoan, Sarcocystis neurona, which have been linked to water-borne outbreaks in humans and wildlife along North America's Pacific Coast. Using genetic tools, we found high rates of protozoal infection, predominantly concomitant infections, in animals inhabiting major waterways of the Pacific Northwest. These dual infections of T. gondii and S. neurona were more frequently associated with mortality and protozoal encephalitis than single infections, indicating a role for polyparasitism in disease severity. Finally, rare T. gondii genotypes linked to a major human outbreak in the Pacific Northwest were abundant in marine mammals of the region, emphasizing wildlife as relevant sentinels for evaluation of human health risks. Our data implicate polyparasitism as a critical factor associated with the severity of protozoal disease. We also identify the need for vigilant surveillance of public waterways to prevent fecal contamination recurrently threatening human and wildlife health along the Pacific coast.

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          Most cited references65

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          A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation.

          We previously developed a cladistic approach to identify subsets of haplotypes defined by restriction endonuclease mapping or DNA sequencing that are associated with significant phenotypic deviations. Our approach was limited to segments of DNA in which little recombination occurs. In such cases, a cladogram can be constructed from the restriction site or sequence data that represents the evolutionary steps that interrelate the observed haplotypes. The cladogram is used to define a nested statistical design to identify mutational steps associated with significant phenotypic deviations. The central assumption behind this strategy is that any undetected mutation causing a phenotypic effect is embedded within the same evolutionary history that is represented by the cladogram. The power of this approach depends upon the confidence one has in the particular cladogram used to draw inferences. In this paper, we present a strategy for estimating the set of cladograms that are consistent with a particular sample of either restriction site or nucleotide sequence data and that includes the possibility of recombination. We first evaluate the limits of parsimony in constructing cladograms. Once these limits have been determined, we construct the set of parsimonious and nonparsimonious cladograms that is consistent with these limits. Our estimation procedure also identifies haplotypes that are candidates for being products of recombination. If recombination is extensive, our algorithm subdivides the DNA region into two or more subsections, each having little or no internal recombination. We apply this estimation procedure to three data sets to illustrate varying degrees of cladogram ambiguity and recombination.
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            Biological and biomedical implications of the co-evolution of pathogens and their hosts.

            Co-evolution between host and pathogen is, in principle, a powerful determinant of the biology and genetics of infection and disease. Yet co-evolution has proven difficult to demonstrate rigorously in practice, and co-evolutionary thinking is only just beginning to inform medical or veterinary research in any meaningful way, even though it can have a major influence on how genetic variation in biomedically important traits is interpreted. Improving our understanding of the biomedical significance of co-evolution will require changing the way in which we look for it, complementing the phenomenological approach traditionally favored by evolutionary biologists with the exploitation of the extensive data becoming available on the molecular biology and molecular genetics of host-pathogen interactions.
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              Incorporating a Rapid-Impact Package for Neglected Tropical Diseases with Programs for HIV/AIDS, Tuberculosis, and Malaria

              Hotez et al. argue that achieving success in the global fight against HIV/AIDS, tuberculosis, and malaria may well require a concurrent attack on the neglected tropical diseases.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                May 2011
                24 May 2011
                : 5
                : 5
                : e1142
                Affiliations
                [1 ]Laboratory of Parasitic Diseases, National Institutes of Health, National Institute of Allergy and Infectious Diseases (NIAID), Bethesda, Maryland, United States of America
                [2 ]Animal Health Centre, Ministry of Agriculture and Food, Abbotsford, British Columbia, Canada
                [3 ]Marine Mammal Research Unit, Fisheries Centre, Aquatic Ecosystems Research Laboratory (AERL), University of British Columbia, Vancouver, British Columbia, Canada
                [4 ]Washington Department of Fish and Wildlife, Lakewood, Washington, United States of America
                [5 ]Cascadia Research Collective, Olympia, Washington, United States of America
                University of California San Diego School of Medicine, United States of America
                Author notes

                Conceived and designed the experiments: MEG AKG SLM. Performed the experiments: AKG SLM. Analyzed the data: AKG SR DML MEG. Contributed reagents/materials/analysis tools: SR DML JH. Wrote the paper: AKG MEG. Performed pathology interpretations: SR DML.

                Article
                PNTD-D-10-00154
                10.1371/journal.pntd.0001142
                3101184
                21629726
                5b3e8521-74dd-44e8-9c83-40842ad4d2fe
                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
                History
                : 8 November 2010
                : 7 March 2011
                Page count
                Pages: 13
                Categories
                Research Article
                Biology
                Genetics
                Population Genetics
                Marine Biology
                Marine Conservation
                Model Organisms
                Protozoan Models
                Population Biology
                Epidemiology
                Infectious Disease Epidemiology
                Population Genetics
                Veterinary Science
                Veterinary Diseases
                Veterinary Parasitology
                Veterinary Epidemiology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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