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. 2022 Dec 19;16(12):e0010974.
doi: 10.1371/journal.pntd.0010974. eCollection 2022 Dec.

Identification of the parasite, Trypanosoma cruzi, in multiple tissues of epidemiological significance in the Virginia opossum (Didelphis virginiana): Implications for environmental and vertical transmission routes

Affiliations

Identification of the parasite, Trypanosoma cruzi, in multiple tissues of epidemiological significance in the Virginia opossum (Didelphis virginiana): Implications for environmental and vertical transmission routes

Carson W Torhorst et al. PLoS Negl Trop Dis. .

Abstract

Background: Trypanosoma cruzi, a parasitic protozoan, is endemic to the Americas and the causative agent of Chagas disease in humans. In South America, opossums facilitate transmission via infected anal gland secretions in addition to transmission via triatomine vectors. In North America, the Virginia opossum is a reservoir host for the parasite with transmission routes that are not clearly defined. The unique biology of this marsupial provides the opportunity to investigate vertical transmission in this wildlife species in situ. Our objectives were to investigate alternative routes of transmission that may facilitate spillover into other species and to determine if vertical transmission was evident.

Methodology/principal findings: Virginia opossums were sampled at 10 trapping locations over a 10-month period in a 5-county region of north central Florida. Peripheral blood, fecal swabs, and anal gland secretions were collected from each adult individual, and peripheral blood was collected from joey opossums. Total DNA was extracted from each collected sample type, and T. cruzi infected individuals and the infecting Discrete Typing Unit (DTU) were identified using real time PCR methods. Adult Virginia opossums (n = 112) were infected with T. cruzi (51.8%, 95% CI [42.6-60.8%]) throughout the sampled period and at each location. T. cruzi DNA was found in each of the three biological sample types. Vertical transmission of T. cruzi was inferred in one litter of mother-dependent (n = 20, 5.0%, 95% CI [0.9-23.6%]) joey opossums where 2 joeys from this same litter were rtPCR positive for T. cruzi.

Conclusions/significance: We inferred vertical transmission from mother to neonate which may serve to amplify the prevalence of T. cruzi in adult Virginia opossums. T. cruzi DNA was detected in the anal gland secretions of Virginia opossums. Infected anal gland secretions suggest a possible environmental route of transmission for T. cruzi via the deposition of contaminated feces and spraint at wildlife latrines. Only DTU1 was identified in the sampled population which is consistent with human autochthonous cases in the United States.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Identification of the locations where Virginia opossums were sampled.
Identification of the 5 counties, sampled location, and nearest city to the sampled location in north central Florida where opossums were live trapped. Map was created using QGIS Geographic Information System version 3.22.5-Białowieża, http://qgis.osgeo.org. County layers map (TIGER/Line Shapefile, 2016, state, Florida, Current County Subdivision State-based) and city locations (TIGER/Line Shapefile, Current, State, Florida, Places) were accessed from the United States Census Bureau, https://catalog.data.gov/dataset.
Fig 2
Fig 2. Opossum feces and anal gland secretion.
Image depicting opossum feces (yellow arrow) contaminated with anal gland secretion (red arrow). Opossum anal gland secretion (blue arrow) can be seen in close association with the fecal bolus that is sitting on the trigger pan of the Tomahawk livetrap. This individual was sampled but negative for T. cruzi. The tail of the Virginia opossum can be seen in the background of the image. (Photo credit: C. W. Torhorst).
Fig 3
Fig 3. Female Virginia opossum and joeys.
A depiction of the marsupium from two adult female Virginia opossums. From the first female, her marsupium, which is expanded to show that it does not contain joeys, and to further detail the cleanliness of the feature and the expanse of the pouch that holds the joeys within (A). From a second female her marsupium gently expanded to expose the mother-dependent joeys held within (B), and from a third female, a mother-dependent joeys with its categorically important features: developing hair, ears, eye openings, while still attached to the mother’s teat (C) (Photo credit: C.W. Torhorst).

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