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Identification of Bloodmeal Sources And Identification of bloodmeal sources and Trypanosoma cruzi infection in triatomine bugs (Hemiptera: Reduviidae) from residential settings in Texas, the United States Sonia A. Kjos, Centers for Disease Control and Prevention Paula L. Marcet, Centers for Disease Control and Prevention Michael J. Yabsley, University of Georgia Uriel Kitron, Emory University Karen F. Snowden, Texas A&M University Kathleen S. Logan, Texas A&M University John C. Barnes, Southwest Texas Veterinary Medical Center Ellen M. Dotson, Centers for Disease Control and Prevention Journal Title: Journal of Medical Entomology Volume: Volume 50, Number 5 Publisher: Oxford University Press (OUP): Policy B - Oxford Open Option D | 2013-09-01, Pages 1126-1139 Type of Work: Article | Post-print: After Peer Review Publisher DOI: 10.1603/ME12242 Permanent URL: https://pid.emory.edu/ark:/25593/v72sq Final published version: http://dx.doi.org/10.1603/ME12242 Copyright information: © 2013 Entomological Society of America. Accessed September 30, 2021 9:56 PM EDT NIH Public Access Author Manuscript J Med Entomol. Author manuscript; available in PMC 2014 May 01. NIH-PA Author ManuscriptPublished NIH-PA Author Manuscript in final edited NIH-PA Author Manuscript form as: J Med Entomol. 2013 September ; 50(5): 1126–1139. Identification of Bloodmeal Sources and Trypanosoma cruzi Infection in Triatomine Bugs (Hemiptera: Reduviidae) From Residential Settings in Texas, the United States SONIA A. KJOS1,2,3, PAULA L. MARCET1, MICHAEL J. YABSLEY4,5, URIEL KITRON6, KAREN F. SNOWDEN7, KATHLEEN S. LOGAN7, JOHN C. BARNES8, and ELLEN M. DOTSON1 1 Division of Parasitic Diseases and Malaria, Entomology Branch, Centers for Disease Control and Prevention, 1600 Clifton Rd., MS G49, Atlanta, GA 30329. 4 Southeastern Cooperative Wildlife Disease Study, Department of Population Health, College of Veterinary Medicine, University of Georgia, Athens, GA 30602. 5 Daniel B. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602. 6 Department of Environmental Studies, Emory University, 400 Dowman Dr., E511 Math and Science Center, Atlanta, GA 30322. 7 Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843-4467. 8 Southwest Texas Veterinary Medical Center, Uvalde, TX 78801. Abstract The host–vector–parasite interactions in Chagas disease peridomestic transmission cycles in the United States are not yet well understood. Trypanosoma cruzi (Kinetoplastida: Trypanosomatidae) infection prevalence and bloodmeal sources were determined for adult and immature triatomine (Hemiptera: Reduviidae) specimens collected from residential settings in central Texas. Sequenced cytochrome b DNA segments obtained from triatomine digestive tract identified nine vertebrate hosts and one invertebrate host in four triatomine species (Triatoma gerstaeckeri, Triatoma indictiva, Triatoma protracta, and Triatoma sanguisuga). The broad range of wild and domestic host species detected in triatomine specimens collected from residential sites indicates high host diversity and potential movement between the sylvatic and peridomestic settings. Domestic dogs appear to be key in the maintenance of the peridomestic transmission cycle as both a blood host for the triatomine vectors and a potential reservoir for the parasite. The high rate of T. cruzi infection among triatomine specimens that were collected from inside houses, outside houses, and dog kennels (69, 81, and 82%, respectively) suggests a current risk for Chagas disease vector-borne transmission for humans and domestic animals in residential settings in Texas because of overlap with the sylvatic cycle. Keywords triatomine; Trypanosoma cruzi; host association; bloodmeal analysis 3 Corresponding author, [email protected].. 2Current address: Department of Biology, University of Minnesota, 207 Swenson Science Bldg, 1035 Kirby Dr., Duluth, MN, 55812-3004. KJOS et al. Page 2 Chagas disease, caused by the hemoflagellate protozoan parasite, Trypanosoma cruzi (Kinetoplastida: Trypanosomatidae), is the most important parasitic disease on the American NIH-PA Author Manuscript NIH-PA Author Manuscriptcontinents, NIH-PA Author Manuscript accounting for an estimated 8 million human infections, with 56,000 new cases and 12,000 deaths annually occurring in Latin American countries (PAHO 2006, World Health Organization [WHO] 2008). Hematophagous triatomine bugs (Hemiptera: Reduviidae: Triatominae) are the biological arthropod vectors of T. cruzi, transmitting the parasite in infectious feces deposited on or near the host during or shortly after the bug feeds. The parasite enters the vertebrate host when the feces contaminate the bite site or mucous membranes. Although vector-borne transmission continues to be the primary route of infection, alternative modes of transmission include blood transfusion, organ transplantation, congenital, and oral ingestion of contaminated foods or drinks (Coura and Dias 2009). Enzootic transmission cycles are endemic across the southern United States, where 24 wildlife mammalian species have been identified as reservoirs, acute and chronic infections have been documented in at least 48 domestic dog breeds, and triatomine vectors have been reported from 28 states (Bern et al. 2011). Of the 141 currently recognized triatomine species, 11 are native to the United States and all are considered potential vectors of Chagas disease (Schofield and Galvao 2009). Although 8 of the 11 species have been associated with human bites in the United States (Packchanian 1940, Wood 1942, Arnold and Bell 1944, Ryckman 1981, Klotz et al. 2010), human T. cruzi infection because of autochthonous vector-borne transmission has been rarely reported. Between 1955 and 2006, seven human cases were reported in two adults and five young children from the states of Texas (n = 4), CA (n = 1), Tennessee (n = 1), and Louisiana (n = 1) (Woody and Woody 1955, Anonymous 1956, Schiffler et al. 1984, Ochs et al. 1996, Herwaldt et al. 2000, Dorn et al. 2007, Kjos et al. 2009). With the exception of one adult case from Louisiana, all infected individuals sought medical attention because of acute symptoms. Since 2007, voluntary testing of donated blood for T. cruzi antibodies in the United States has identified >1,600 confirmed seropositive donations (AABB 2012). Although most seropositive donors are Latin American immigrants who likely acquired the infection before relocating to the United States, a subset of these seropositive donors were U.S.-born with no travel history to endemic areas (Bern et al. 2008). A recent study of confirmed seropositive U.S. blood donors identified 16 additional autochthonous cases, all asymptomatic chronic infections, presumably acquired by vector-borne transmission in the United States (Cantey et al. 2012). The predominant risk factors included living in a southern state where triatomine vectors or infected mammalian reservoirs had been reported and participation in outdoor activities. Documentation of human–triatomine encounters in the United States predates the discovery of the T. cruzi vector-borne transmission cycle (Leconte 1855, Kimball 1894), and these encounters continue to be reported today primarily in association with allergic reactions to triatomine bites (Klotz et al. 2010, Reisenman et al. 2010). The frequency of human–triatomine encounters in the United States is considerably lower than in areas with high vector-borne transmission rates in Latin America, presumably because of the uncommon occurrence of triatomine colonization of U.S. houses. However, the compelling evidence for vector-borne transmission in newly diagnosed chronic cases among blood donors suggests vector-borne transmission may occur more frequently in the United States than previously recognized, particularly because acute infection is very mild or asymptomatic in most immunocompetent individuals (Rassi et al. 2010). Whereas autochthonous human T. cruzi infections in the United States are rarely reported, acute and chronic cases among domestic dogs have been documented widely across the southern states, beginning with Texas in 1972 (Williams et al. 1977, Tomlinson et al. 1981, Barr et al. 1991, Duprey et al. 2006, Kjos et al. 2008, Rowland et al. 2010). The disparity in reported infection prevalence between humans and dogs in the United States is likely because of differences in vector exposure levels and transmission routes, as well as an J Med Entomol. Author manuscript; available in PMC 2014 May 01. KJOS et al. Page 3 increasing awareness among veterinarians of the potential risk of infection for dogs and therefore increased testing (Kjos et al. 2008) in contrast to the lack of awareness of human NIH-PA Author Manuscript NIH-PA Author Manuscriptrisk among NIH-PA Author Manuscript physicians (Stimpert and Montgomery 2010, Verani et al. 2010). The presence of infected domestic animals in peridomestic and domestic settings, particularly dogs, is a significant contributor to human infection in certain areas of South America, with dogs serving both as blood hosts for the triatomine vectors and as parasite reservoirs (Gürtler et al. 1986, 1996, 2007). Dogs housed in proximity to two U.S. human autochthonous cases tested positive for T. cruzi antibodies, providing some evidence of a potential role for dogs in human risk in the United States (Navin et al. 1985, Herwaldt et al. 2000). Recent studies of T. cruzi infection in triatomine specimens collected in and around houses
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