Toward an Ecological Framework for Assessing Reservoirs of Vector-Borne Pathogens: Wildlife Reservoirs of Trypanosoma cruzi across the Southern United States

Abstract

Wildlife species are critical for both feeding vectors and serving as reservoirs of zoonotic vector-borne pathogens. Transmission pathways leading to disease in humans or other target taxa might be better understood and managed given a complete understanding of the relative importance of different reservoir species in nature. Using the conceptual framework of “reservoir potential,” which considers elements of both reservoir competence and vector-host contact, we review the wildlife reservoirs of Trypanosoma cruzi in the southern United States, where many species of triatomine vectors occur and wildlife maintain enzootic cycles that create a risk of spillover to humans, domestic dogs, and captive nonhuman primates that may develop Chagas disease. We reviewed 77 published reports of T. cruzi infection in at least 26 wildlife species across 15 southern states. Among the most well-studied and highly infected reservoirs are raccoon (Procyon lotor), woodrat (Neotoma spp.), and opossum (Didelphis virginiana), with aggregate overall infection prevalences of 36.4, 34.7, and 22.9%, respectively. Just over 60% of studies utilized methods from which an infectiousness index could be generated and show that raccoons and striped skunk (Mephitis mephitis) are among the most infectious wildlife hosts. Triatomine-host contact has sparsely been quantified in the southern United States, but 18 of the 24 host species previously identified to have been fed upon by triatomines are wildlife. Future studies to parameterize the reservoir potential model, especially to quantify wildlife infectiousness, vector-host contact, and the epidemiological importance of parasite strains maintained by wildlife, could open new doors for managing enzootic cycles and reducing T. cruzi spillover risk.

Trypanosoma cruzi Transmission Among Captive Nonhuman Primates, Wildlife, and Vectors

“…Recognition of the associations between parasite DTU and reservoir host species may have important implications for public or veterinary health (Bern et al 2011 ; Jansen et al 2017 ; Hodo and Hamer 2017 ). We found that NHPs were infected almost equally with both TcI and TcIV, whereas the small numbers of raccoons and opossums exclusively harbored TcIV and TcI, respectively—host associations that have been previously shown (Bern et al 2011 ; Roellig et al 2013 ).…”

“…in the USA (Packchanian 1942 ; Charles et al 2012 ), and several studies have reported T. cruzi infection in other species of rodents (Burkholder et al 1980 ; Navin et al 1985 ; Charles et al 2012 ; Herrera et al 2015 ; Aleman et al 2017 ). T. cruzi transmission cycles are characterized by regional heterogeneity, and the important reservoirs likely differ across geographical areas (Hodo and Hamer 2017 ). Because the mammal traps were not placed randomly or systematically along transects, the species and numbers of mammals captured are not necessarily reflective of the entire population structure of the wildlife community.…”

“…T. cruzi is divided into 7 genetic strain types or discrete typing units (DTUs): TcI–TcVI and TcBat, which are reportedly associated with differing clinical manifestations, reservoir host species, and geographical locations (Barr et al 1991a , b ; Ramírez et al 2010 ; Duz et al 2014 ; Jansen et al 2015 ). In the USA, TcI and TcIV are the most commonly reported DTUs (Bern et al 2011 ; Roellig et al 2013 ), and diverse mammalian wildlife species serve as reservoirs (Bern et al 2011 ; Zeledón et al 2012 ; Hodo and Hamer 2017 ).…”

Comparison of the Bacterial Gut Microbiome of North American Triatoma spp. With and Without Trypanosoma cruzi

“…Although triatomines found in the United States are generally considered sylvatic, these vectors are regularly encountered in and around human dwellings (Kjos et al, 2008;Wozniak et al, 2015;Curtis-Robles et al, 2018b). Wildlife and domestic canines are infected with T. cruzi throughout Texas and across the southern United States (Beard et al, 2003;Kjos et al, 2008;Brown et al, 2010;Curtis-Robles et al, 2017;Hodo and Hamer, 2017).…”

Peer Review #1 of "Sylvatic host associations of Triatominae and implications for Chagas disease reservoirs: a review and new host records based on archival specimens (v0.2)"

“…is higher than we expected as these species tend to be thought of as minor hosts for Triatominae or are primarily associated only with certain species [42]. This discrepancy may reflect that these hosts are not known to be able to harbor the T. cruzi pathogen [59,60] is that oral transmission in the sylvatic cycle may be the primary mechanism of parasite spread [62] and some insectivorous mammals often have a higher prevalence of the disease [63]. It has been reported that even T. cruzi-infected vertebrates eaten as prey can be infective [64] and it appears that Chagas disease can "bioaccumulate" in predators including highly carnivorous top predators (e.g., ocelots), that are nocturnal without permanent dens and are thus unlikely to be exposed to feeding Triatominae [65].…”