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.
Highlights
A single individual often plays host to one, but to an entire community of parasites [1,2,3], and this polyparasitism has been identified as a critical factor in determining the virulence of an infection [4,5,6]
We investigate polyparasitism as one factor governing the spectrum of disease in Toxoplasma gondii infections
We found high rates of protozoal infection, predominantly concomitant infections, in animals inhabiting major waterways of the Pacific Northwest
Summary
A single individual often plays host to one, but to an entire community of parasites [1,2,3], and this polyparasitism has been identified as a critical factor in determining the virulence of an infection [4,5,6]. Type II and III infections in mice are classified as avirulent and Type I as acutely virulent [9,10]. Studies have increasingly questioned this strict dichotomy [11]; mouse virulent Type II strains and avirulent Type I-like strains have been discovered [12,13], while acute human toxoplasmosis is commonly attributed to Type II and atypical strains [7,8,11,14,15,16]. Significant mortality of Southern sea otters (Enhydra lutris nereis) between 1998 and 2004 was exclusively associated with Type II and Type X, a novel clade of strains first identified in sea otters [17]
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