Southern Plains Woodrats (Neotoma micropus) from Southern Texas Are Important Reservoirs of Two Genotypes of Trypanosoma cruzi and Host of a Putative Novel Trypanosoma Species

Abstract

Trypanosoma cruzi, the causative agent of Chagas' disease, is an important public health and veterinary pathogen. Although human cases are rare in the United States, infections in wildlife, and in some areas domestic dogs, are common. In 2008 and 2010, we investigated T. cruzi prevalence in possible vertebrate reservoirs in southern Texas, with an emphasis on southern plains woodrats (Neotoma micropus). Infection status was determined using a combination of culture isolation, polymerase chain reaction (PCR), and serologic testing. Based on PCR and/or culture, T. cruzi was detected in 35 of 104 (34%) woodrats, 3 of 4 (75%) striped skunks (Mephitis mephitis), 12 of 20 (60%) raccoons (Procyon lotor), and 5 of 28 (18%) other rodents including a hispid cotton rat (Sigmodon hispidus), rock squirrel (Otospermophilus variegatus), black rat (Rattus rattus), and two house mice (Mus musculus). Additionally, another Trypanosoma species was detected in 41 woodrats, of which 27 were co-infected with T. cruzi. Genetic characterization of T. cruzi revealed that raccoon, rock squirrel, and cotton rat isolates were genotype TcIV, while woodrats and skunks were infected with TcI and TcIV. Based on the Chagas Stat-Pak assay, antibodies were detected in 27 woodrats (26%), 13 raccoons (65%), 4 skunks (100%), and 5 other rodents (18%) (two white-ankled mice [Peromyscus pectoralis laceianus], two house mice, and a rock squirrel). Seroprevalence based on indirect immunofluorescence antibody testing was higher for both woodrats (37%) and raccoons (90%), compared with the Chagas Stat-Pak. This is the first report of T. cruzi in a hispid cotton rat, black rat, rock squirrel, and white-ankled mouse. These data indicate that based on culture and PCR testing, the prevalence of T. cruzi in woodrats is comparable with other common reservoirs (i.e., raccoons and opossums) in the United States. However, unlike raccoons and opossums, which tend to be infected with a particular genotype, southern plains woodrats were infected with TcI and TcIV at near equal frequencies.

The role of the ratio of vector and host densities in the evolution of transmission modes in vector-borne diseases. The example of sylvatic Trypanosoma cruzi

“…If we consider the threshold vectorhost ratios for saturation of the contact processes provided above, we obtain for woodrats a situation Q h < Q < Q v , in which the vector/host ratio can shift the advantage from one strain to the other. This is in accordance with the fact that both T. cruzi strains have been observed in woodrats in South Texas [39]. For raccoons and opossums, these estimations lead to Q h < Q v < Q.…”

The role of adaptations in two-strain competition for sylvaticTrypanosoma cruzitransmission

“…Further study of this competition using stochastic and/or multi-host models is warranted by reports of prevalence of T. cruzi I -at trace levels in raccoons [39] and more widespread among woodrats [5] -in transmission cycles where T. cruzi IV is established as enzootic. Although the deterministic model developed in this study predicts competitive exclusion, stochastic models can show how fluctuations in transient dynamics (which may last many years) can slow or even reverse its outcome on a local scale, allowing a strain to persist (and even displace another) when it would be normally expected to die out.…”

“…Table A1 provides estimates of T. cruzi infection prevalence in the various host and vector species, also taken from [23]. Note that studies reviewed in [23] which provided prevalence estimates did not identify parasite type or strain; although opossums are associated exclusively with T. cruzi I in the USA, while raccoons are associated with T. cruzi IIa, both strains have been found to be enzootic in woodrats, at roughly equal levels [5]. Vectors are presumably infected with the same strains as their respective hosts.…”

“…Other sylvatic US hosts, including raccoons (as well as skunks, foxes, and armadillos), are associated instead with T. cruzi IV [17,39]. Most recently, both strains have been found in Texas woodrats [5].…”

Graphical analysis of evolutionary trade-off in sylvatic Trypanosoma cruzi transmission modes

“…At the same time, raccoons (Procyon lotor) there are found infected almost exclusively with T. cruzi IV, at a high prevalence (typically 50% or higher) [22]; T. cruzi I persists primarily in opossums (Didelphis marsupialis) in the southeastern United States (SE US), who are immune to T. cruzi IV [23]. In Texas and northern Mexico, meanwhile, both strains are found at roughly equal levels in woodrats (Neotoma micropus) [4]. T. cruzi I is often described as chagasic and more virulent (see, e.g., [19]) compared to T. cruzi IV, which has been found to be better adapted to vertical transmission [11], and the importance of vertical and oral transmission in an epidemiological landscape where classical stercorarian transmission is disadvantaged almost surely plays a role in mediating interstrain competition here.…”