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. 2012;7(9):e46013.
doi: 10.1371/journal.pone.0046013. Epub 2012 Sep 26.

Ecological connectivity of Trypanosoma cruzi reservoirs and Triatoma pallidipennis hosts in an anthropogenic landscape with endemic Chagas disease

Janine M Ramsey  1 , Ana E Gutiérrez-Cabrera, Liliana Salgado-Ramírez, A Townsend Peterson, Victor Sánchez-Cordero, Carlos N Ibarra-Cerdeña
Affiliations

Ecological connectivity of Trypanosoma cruzi reservoirs and Triatoma pallidipennis hosts in an anthropogenic landscape with endemic Chagas disease

Janine M Ramsey et al. PLoS One. 2012.

Abstract

Traditional methods for Chagas disease prevention are targeted at domestic vector reduction, as well as control of transfusion and maternal-fetal transmission. Population connectivity of Trypanosoma cruzi-infected vectors and hosts, among sylvatic, ecotone and domestic habitats could jeopardize targeted efforts to reduce human exposure. This connectivity was evaluated in a Mexican community with reports of high vector infestation, human infection, and Chagas disease, surrounded by agricultural and natural areas. We surveyed bats, rodents, and triatomines in dry and rainy seasons in three adjacent habitats (domestic, ecotone, sylvatic), and measured T. cruzi prevalence, and host feeding sources of triatomines. Of 12 bat and 7 rodent species, no bat tested positive for T. cruzi, but all rodent species tested positive in at least one season or habitat. Highest T. cruzi infection prevalence was found in the rodents, Baiomys musculus and Neotoma mexicana. In general, parasite prevalence was not related to habitat or season, although the sylvatic habitat had higher infection prevalence than by chance, during the dry season. Wild and domestic mammals were identified as bloodmeals of T. pallidipennis, with 9% of individuals having mixed human (4.8% single human) and other mammal species in bloodmeals, especially in the dry season; these vectors tested >50% positive for T. cruzi. Overall, ecological connectivity is broad across this matrix, based on high rodent community similarity, vector and T. cruzi presence. Cost-effective T. cruzi, vector control strategies and Chagas disease transmission prevention will need to consider continuous potential for parasite movement over the entire landscape. This study provides clear evidence that these strategies will need to include reservoir/host species in at least ecotones, in addition to domestic habitats.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Orthophoto of the Chalcatzingo, Morelos, Mexico, landscape and sample transects (white lines) in each habitat: (A) domestic, (B) ecotone (crop areas), and (C) sylvatic.
Landscape classification is qualitative given differences among the habitats: in the domestic area only houses and their corresponding gardens are available with 13% of households maintaining farm animals; in the ecotone, only crops, animal corrals or grazing areas are available, and in the sylvatic area, no housing, crops or grazing areas are not present, and low deciduous forest principally conserved.
Figure 2
Figure 2. PCR diagnosis of Trypanosoma cruzi in mammals and T. pallidipennis, and bug bloodmeal content.
( A ) Identification of Trypanosoma cruzi (120 bp) and amplification of animal cytochrome b (420 bp) from rodent specimens as DNA positive control: (3–5) Neotoma mexicana, (6–8) Sigmodon hispidus, (9–16) Baiomys musculus, (17–19) Mus musculus, (20) Rattus rattus, (21, 22) Liomys irruratus, (23, 24) Peromyscus levipes. Lanes 2, 3, 5, 6, 8, 14, 15, 16, 18, 19, 20, 21, and 23 were positive for Trypanosoma cruzi. ( B ) Triatoma pallidipennis bloodmeal identification using cytochrome b sequencing. Human blood amplified a 320 bp sequence (lanes 8 to 11), while all animal blood amplified a 420 bp sequence (lanes 2 to 8 and 11). Animal sequences amplified were later sequenced as Didelphis virginiana from an adult female (lane 2), Canis familiaris from a stage 2 nymph (lane 3), Felis catus from a stage 5 nymph (lane 4-), Gallus gallus from a male (lane 5), Sigmodon hispidus from a female (lane 6), Mus musculus from a stage 5 nymph (lane 7), S. hispidus and human from a stage 3 nymph (lane 8), Human from a female (lane 9), human from a stage 5 nymph (lane 10), M. musculus and human from a female (lane 11). PCR conditions allowed double bloodmeal amplification (lane 8 and 11). Lanes 1 and 12 are molecular weight markers.
Figure 3
Figure 3. Correlation analysis between rodent relative abundance (proportional abundance of each species), and Trypanosoma cruzi prevalence (proportion of infected individuals of each species).
Figure 4
Figure 4. Association between reservoir species' relative abundance and their relative Trypanosoma cruzi infection rates and prevalence for (1) Baiomys musculus, (2) Liomys irroratus, (3) Mus musculus, (4) Neotoma mexicana, (5) Peromyscus levipes, (6) Rattus rattus, and (7) Sigmodon hispidus, over both seasons and in all three habitat types.
Figure 5
Figure 5. Trypanosoma cruzi infection rates in Triatoma pallidipennis nymphs and adults collected from sylvatic, ecotone, and domestic habitats in Chalcatzingo.
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Grants and funding

This study was funded by the Secretaria de Salud and Consejo Nacional de Ciencia y Tecnología (CONACyt) project MOR-2004-CO2-012 to JMR, and by the Universidad Nacional Autónoma de México (PAPIIT project 225408 to VS-C, and the Sistema de Informática para la Biodiversidad y el Ambiente [SIBA], and Tecnologías para la Universidad de la Información y la Computación. AEGC was funded with a scholarship from CONACyT for a M. Sc. degree in vector-borne diseases at the Instituto Nacional de Salud Publica. CNIC is funded with a scholarship from CONACyT for studies at the graduate program in Biomedical Sciences of the Universidad Nacional Autonoma de Mexico. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.