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Polyparasitism is associated with increased disease severity in Toxoplasma gondii-infected marine sentinel species.

Gibson AK, Raverty S, Lambourn DM, Huggins J, Magargal SL, Grigg ME - PLoS Negl Trop Dis (2011)

Bottom Line: Genetic typing identified a novel Toxoplasma gondii strain linked to the outbreak, in which a wide spectrum of human disease was observed.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Parasitic Diseases, National Institutes of Health, National Institute of Allergy and Infectious Diseases (NIAID), Bethesda, Maryland, USA.

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.

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Related in: MedlinePlus

Type I alleles dominate Toxoplasma gondii genotypes infecting marine mammals of the Pacific Northwest.Network diagrams of genotyped T. gondii infections at the B1 (n = 70) (A) and NTS2 (n = 72) (B) loci. Chart size is directly proportional to the allele frequency. A single solid circle marks one individual. A single black bar indicates one nucleotide change; a kinked bar indicates that 2 nucleotide changes distinguish alleles. Colors and shadings are used to denote the host species from which a given allele was genotyped. Shades of blue indicate species from the suborder Pinnipedia: Harbor seal (royal blue), Guadalupe fur seal (pale blue), Steller sea lion (sky blue), and Elephant seal (teal). Shades of red mark species from the order Cetacea: Harbor porpoise (red), Killer whale (rose), and Pygmy sperm whale (maroon). Yellow denotes alleles derived from infections of Northern sea otters. Frameworks for diagrams were constructed in TCS v1.21.
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pntd-0001142-g006: Type I alleles dominate Toxoplasma gondii genotypes infecting marine mammals of the Pacific Northwest.Network diagrams of genotyped T. gondii infections at the B1 (n = 70) (A) and NTS2 (n = 72) (B) loci. Chart size is directly proportional to the allele frequency. A single solid circle marks one individual. A single black bar indicates one nucleotide change; a kinked bar indicates that 2 nucleotide changes distinguish alleles. Colors and shadings are used to denote the host species from which a given allele was genotyped. Shades of blue indicate species from the suborder Pinnipedia: Harbor seal (royal blue), Guadalupe fur seal (pale blue), Steller sea lion (sky blue), and Elephant seal (teal). Shades of red mark species from the order Cetacea: Harbor porpoise (red), Killer whale (rose), and Pygmy sperm whale (maroon). Yellow denotes alleles derived from infections of Northern sea otters. Frameworks for diagrams were constructed in TCS v1.21.

Mentions: DNA sequences for one to three T. gondii loci (B1, NTS2, SAG1) were obtained for 85 individuals. Thirty-seven (45%) possessed alleles consistent with a Type I or Type I-like genotype (Table S2), and Type I and Type-I like alleles dominated at the B1 (42/74, 57%) and NTS2 loci (41/78, 53%). (Fig. 6, Table S2). Figure 6 shows a network estimation diagram, generated in TCS v1.21, of the relationships between the alleles in the T. gondii population; the direct proportionality of chart size to allele frequency reveals the over-representation of Type I alleles at both the B1 and NTS2 loci. At the B1 locus, 23% (17/74) of infections carried Type II/III or II/III-like alleles and 20% (15/74) were characterized by Type X or X-like alleles. Type II/III alleles represented 26% (20/78) of alleles at the NTS2 locus, and Type X or X-like alleles represented 21% (16/78) (Table S2). Independent amplifications of multiple tissues per animal demonstrated definitively that 11 individuals (13%) were infected by multiple genotypes possessing distinct tissue tropisms. An additional 22 individuals (26%) were infected by multiple genotypes or by single genotypes harboring unique alleles; our typing analyses were not capable of readily distinguishing between these alternatives (Table S2).


Polyparasitism is associated with increased disease severity in Toxoplasma gondii-infected marine sentinel species.

Gibson AK, Raverty S, Lambourn DM, Huggins J, Magargal SL, Grigg ME - PLoS Negl Trop Dis (2011)

Type I alleles dominate Toxoplasma gondii genotypes infecting marine mammals of the Pacific Northwest.Network diagrams of genotyped T. gondii infections at the B1 (n = 70) (A) and NTS2 (n = 72) (B) loci. Chart size is directly proportional to the allele frequency. A single solid circle marks one individual. A single black bar indicates one nucleotide change; a kinked bar indicates that 2 nucleotide changes distinguish alleles. Colors and shadings are used to denote the host species from which a given allele was genotyped. Shades of blue indicate species from the suborder Pinnipedia: Harbor seal (royal blue), Guadalupe fur seal (pale blue), Steller sea lion (sky blue), and Elephant seal (teal). Shades of red mark species from the order Cetacea: Harbor porpoise (red), Killer whale (rose), and Pygmy sperm whale (maroon). Yellow denotes alleles derived from infections of Northern sea otters. Frameworks for diagrams were constructed in TCS v1.21.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3101184&req=5

pntd-0001142-g006: Type I alleles dominate Toxoplasma gondii genotypes infecting marine mammals of the Pacific Northwest.Network diagrams of genotyped T. gondii infections at the B1 (n = 70) (A) and NTS2 (n = 72) (B) loci. Chart size is directly proportional to the allele frequency. A single solid circle marks one individual. A single black bar indicates one nucleotide change; a kinked bar indicates that 2 nucleotide changes distinguish alleles. Colors and shadings are used to denote the host species from which a given allele was genotyped. Shades of blue indicate species from the suborder Pinnipedia: Harbor seal (royal blue), Guadalupe fur seal (pale blue), Steller sea lion (sky blue), and Elephant seal (teal). Shades of red mark species from the order Cetacea: Harbor porpoise (red), Killer whale (rose), and Pygmy sperm whale (maroon). Yellow denotes alleles derived from infections of Northern sea otters. Frameworks for diagrams were constructed in TCS v1.21.
Mentions: DNA sequences for one to three T. gondii loci (B1, NTS2, SAG1) were obtained for 85 individuals. Thirty-seven (45%) possessed alleles consistent with a Type I or Type I-like genotype (Table S2), and Type I and Type-I like alleles dominated at the B1 (42/74, 57%) and NTS2 loci (41/78, 53%). (Fig. 6, Table S2). Figure 6 shows a network estimation diagram, generated in TCS v1.21, of the relationships between the alleles in the T. gondii population; the direct proportionality of chart size to allele frequency reveals the over-representation of Type I alleles at both the B1 and NTS2 loci. At the B1 locus, 23% (17/74) of infections carried Type II/III or II/III-like alleles and 20% (15/74) were characterized by Type X or X-like alleles. Type II/III alleles represented 26% (20/78) of alleles at the NTS2 locus, and Type X or X-like alleles represented 21% (16/78) (Table S2). Independent amplifications of multiple tissues per animal demonstrated definitively that 11 individuals (13%) were infected by multiple genotypes possessing distinct tissue tropisms. An additional 22 individuals (26%) were infected by multiple genotypes or by single genotypes harboring unique alleles; our typing analyses were not capable of readily distinguishing between these alternatives (Table S2).

Bottom Line: Genetic typing identified a novel Toxoplasma gondii strain linked to the outbreak, in which a wide spectrum of human disease was observed.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Parasitic Diseases, National Institutes of Health, National Institute of Allergy and Infectious Diseases (NIAID), Bethesda, Maryland, USA.

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.

Show MeSH
Related in: MedlinePlus