1932

Abstract

Chagas disease, a neglected tropical disease present in the Americas, is caused by the parasite and is transmitted by triatomine kissing bug vectors. Hundreds of vertebrate host species are involved in the ecology of Chagas disease. The sylvatic nature of most triatomines found in the United States accounts for high levels of animal infections but few reports of human infections. This review focuses on triatomine distributions and animal infections in the southern United States. A quantitative synthesis of available US data from triatomine bloodmeal analysis studies shows that dogs, humans, and rodents are key taxa for feeding triatomines. Imperfect and unvalidated diagnostic tools for wildlife complicate the study of animal infections, and integrated vector management approaches are needed to reduce parasite transmission in nature. The diversity of animal species involved in Chagas disease ecology underscores the importance of a One Health approach for disease research and management.

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2022-02-15
2024-12-05
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Literature Cited

  1. 1. 
    World Health Organ 2015. Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Wkly. Epidemiol. Rec. 6:33–34
    [Google Scholar]
  2. 2. 
    Bern C, Montgomery SP. 2009. An estimate of the burden of Chagas disease in the United States. Clin. Infect. Dis. 49:e52–54
    [Google Scholar]
  3. 3. 
    Beatty NL, Klotz SA. 2020. Autochthonous Chagas disease in the United States: How are people getting infected?. Am. J. Trop. Med. Hyg. 103:967–69
    [Google Scholar]
  4. 4. 
    Lynn MK, Bossak BH, Sandifer PA, Watson A, Nolan MS. 2020. Contemporary autochthonous human Chagas disease in the USA. Acta Trop 205:105361
    [Google Scholar]
  5. 5. 
    Rassi A, Rassi A, Marin-Neto JA. 2010. Chagas disease. Lancet 375:1388–402
    [Google Scholar]
  6. 6. 
    Bern C. 2015. Chagas’ disease. N. Engl. J. Med. 373:456–66
    [Google Scholar]
  7. 7. 
    Bern C, Kjos S, Yabsley MJ, Montgomery SP. 2011. Trypanosoma cruzi and Chagas’ disease in the United States. Clin. Microbiol. Rev. 24:655–81
    [Google Scholar]
  8. 8. 
    Valdez-Tah A, Ibarra-Cerdeña CN. 2021. Call to action: a literature review of Chagas disease risk in California 1916–2018. PLOS Negl. Trop. Dis. 15:e0009035
    [Google Scholar]
  9. 9. 
    Echeverria LE, Morillo CA. 2019. American trypanosomiasis (Chagas disease). Infect. Dis. Clin. N. Am. 33:119–34
    [Google Scholar]
  10. 10. 
    Bonney KM. 2014. Chagas disease in the 21st century: A public health success or an emerging threat?. Parasite 21:11
    [Google Scholar]
  11. 11. 
    Hotez PJ, Dumonteil E, Betancourt Cravioto M, Bottazzi ME, Tapia-Conyer R et al. 2013. An unfolding tragedy of Chagas disease in North America. PLOS Negl. Trop. Dis. 7:e2300
    [Google Scholar]
  12. 12. 
    Garcia MN, Woc-Colburn L, Aguilar D, Hotez PJ, Murray KO. 2015. Historical perspectives on the epidemiology of human Chagas disease in Texas and recommendations for enhanced understanding of clinical Chagas disease in the southern United States. PLOS Negl. Trop. Dis. 9:e0003981
    [Google Scholar]
  13. 13. 
    Bern C, Messenger LA, Whitman JD, Maguire JH 2019. Chagas disease in the United States: a public health approach. Clin. Microbiol. Rev. 33:e00023-19
    [Google Scholar]
  14. 14. 
    Barr SC. 2009. Canine Chagas’ disease (American trypanosomiasis) in North America. Vet. Clin. N. Am. Small Anim. Pract. 39:1055–64 v–vi
    [Google Scholar]
  15. 15. 
    Barr SC, Gossett KA, Klei TR. 1991. Clinical, clinicopathologic, and parasitologic observations of trypanosomiasis in dogs infected with North American Trypanosoma cruzi isolates. Am. J. Vet. Res. 52:954–60
    [Google Scholar]
  16. 16. 
    Roellig DM, Ellis AE, Yabsley MJ. 2009. Oral transmission of Trypanosoma cruzi with opposing evidence for the theory of carnivory. J. Parasitol. 95:360–64
    [Google Scholar]
  17. 17. 
    Velásquez-Ortiz N, Ramírez JD. 2020. Understanding the oral transmission of Trypanosoma cruzi as a veterinary and medical foodborne zoonosis. Res. Vet. Sci. 132:448–61
    [Google Scholar]
  18. 18. 
    Montenegro VM, Jiménez M, Dias JC, Zeledón R. 2002. Chagas disease in dogs from endemic areas of Costa Rica. Mem. Inst. Oswaldo Cruz 97:491–94
    [Google Scholar]
  19. 19. 
    Jansen AM, Xavier SCC, Roque ALR. 2015. The multiple and complex and changeable scenarios of the Trypanosoma cruzi transmission cycle in the sylvatic environment. Acta Trop 151:1–15
    [Google Scholar]
  20. 20. 
    Ramírez JD, Guhl F, Rendón LM, Rosas F, Marin-Neto JA, Morillo CA. 2010. Chagas cardiomyopathy manifestations and Trypanosoma cruzi genotypes circulating in chronic Chagasic patients. PLOS Negl. Trop. Dis. 4:e899
    [Google Scholar]
  21. 21. 
    Zingales B, Miles MA, Campbell DA, Tibayrenc M, Macedo AM et al. 2012. The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infect. Genet. Evol. 12:240–53
    [Google Scholar]
  22. 22. 
    Herrera C, Majeau A, Didier P, Falkenstein KP, Dumonteil E. 2019. Trypanosoma cruzi diversity in naturally infected nonhuman primates in Louisiana assessed by deep sequencing of the mini-exon gene. Trans. R. Soc. Trop. Med. Hyg. 113:281–86
    [Google Scholar]
  23. 23. 
    Dumonteil E, Pronovost H, Bierman EF, Sanford A, Majeau A et al. 2020. Interactions among Triatoma sanguisuga blood feeding sources, gut microbiota and Trypanosoma cruzi diversity in southern Louisiana. Mol. Ecol. 29:3747–61
    [Google Scholar]
  24. 24. 
    Dumonteil E, Desale H, Tu W, Duhon B, Wolfson W et al. 2021. Shelter cats host infections with multiple Trypanosoma cruzi discrete typing units in southern Louisiana. Vet. Res. 52:53
    [Google Scholar]
  25. 25. 
    Dumonteil E, Elmayan A, Majeau A, Tu W, Duhon B et al. 2020. Genetic diversity of Trypanosoma cruzi parasites infecting dogs in southern Louisiana sheds light on parasite transmission cycles and serological diagnostic performance. PLOS Negl. Trop. Dis. 14:e0008932
    [Google Scholar]
  26. 26. 
    Zingales B. 2018. Trypanosoma cruzi genetic diversity: something new for something known about Chagas disease manifestations, serodiagnosis and drug sensitivity. Acta Trop 184:38–52
    [Google Scholar]
  27. 27. 
    Ceccarelli S, Balsalobre A, Medone P, Cano ME, Gurgel Gonçalves R et al. 2018. DataTri, a database of American triatomine species occurrence. Sci. Data. 5:180071
    [Google Scholar]
  28. 28. 
    Justi SA, Galvão C. 2017. The evolutionary origin of diversity in Chagas disease vectors. Trends Parasitol. 33:42–52
    [Google Scholar]
  29. 29. 
    Curtis-Robles R, Auckland LD, Snowden KF, Hamer GL, Hamer SA. 2018. Analysis of over 1500 triatomine vectors from across the US, predominantly Texas, for Trypanosoma cruzi infection and discrete typing units. Infect. Genet. Evol. 58:171–80
    [Google Scholar]
  30. 30. 
    Curtis-Robles R, Hamer SA, Lane S, Levy MZ, Hamer GL 2018. Bionomics and spatial distribution of triatomine vectors of Trypanosoma cruzi in Texas and other southern states, USA. Am. J. Trop. Med. Hyg. 98:113–21
    [Google Scholar]
  31. 31. 
    Eggers P, Offutt-Powell T, Lopez K, Montgomery S, Lawrence G. 2019. Notes from the field: identification of a Triatoma sanguisuga “kissing bug”—Delaware, 2018. Morb. Mortal. Wkly. Rep. 68:359
    [Google Scholar]
  32. 32. 
    Nielsen DH, Koch K, Roachell W, Delgado B, Bast J. 2021. First record of an established population of Triatoma sanguisuga (Hemiptera: Reduviidae) in Richardson County, Nebraska. J. Med. Entomol. 2021:tjab122
    [Google Scholar]
  33. 33. 
    Browne AJ, Guerra CA, Alves RV, da Costa VM, Wilson AL et al. 2017. The contemporary distribution of Trypanosoma cruzi infection in humans, alternative hosts and vectors. Sci. Data 4:170050
    [Google Scholar]
  34. 34. 
    Martínez-Ibarra JA, Alejandre-Aguilar R, Paredes-González E, Martínez-Silva MA, Solorio-Cibrián M et al. 2007. Biology of three species of North American Triatominae (Hemiptera: Reduviidae: Triatominae) fed on rabbits. Mem. Inst. Oswaldo Cruz 102:925–30
    [Google Scholar]
  35. 35. 
    Georgieva AY, Gordon ERL, Weirauch C 2017. Sylvatic host associations of Triatominae and implications for Chagas disease reservoirs: a review and new host records based on archival specimens. PeerJ 5:e3826
    [Google Scholar]
  36. 36. 
    Pippin WF. 1970. The biology and vector capability of Triatoma sanguisuga texana Usinger and Triatoma gerstaeckeri (Stal) compared with Rhodnius prolixus (Stal) (Hemiptera: Triatominae). J. Med. Entomol. 7:30–45
    [Google Scholar]
  37. 37. 
    Gürtler RE, Fernandez MDP, Cecere MC, Cohen JE 2017. Body size and hosts of Triatoma infestans populations affect the size of bloodmeal contents and female fecundity in rural northwestern Argentina. PLOS Negl. Trop. Dis. 11:e0006097
    [Google Scholar]
  38. 38. 
    Cordero-Montoya G, Flores-Villegas AL, Salazar-Schettino PM, Vences-Blanco MO, Rocha-Ortega M et al. 2019. The cost of being a killer's accomplice: Trypanosoma cruzi impairs the fitness of kissing bugs. Parasitol. Res. 118:2523–29
    [Google Scholar]
  39. 39. 
    Botto-Mahan C, Cattan PE, Medel R. 2006. Chagas disease parasite induces behavioural changes in the kissing bug Mepraia spinolai. Acta Trop 98:219–23
    [Google Scholar]
  40. 40. 
    Wormington JD, Gillum C, Meyers AC, Hamer GL, Hamer SA. 2018. Daily activity patterns of movement and refuge use in Triatoma gerstaeckeri and Rhodnius prolixus (Hemiptera: Reduviidae), vectors of the Chagas disease parasite. Acta Trop 185:301–6
    [Google Scholar]
  41. 41. 
    Hodo CL, Hamer SA. 2017. Toward an ecological framework for assessing reservoirs of vector-borne pathogens: wildlife reservoirs of Trypanosoma cruzi across the southern United States. ILAR J 58:379–92
    [Google Scholar]
  42. 42. 
    Klotz SA, Dorn PL, Mosbacher M, Schmidt JO. 2014. Kissing bugs in the United States: risk for vector-borne disease in humans. Environ. Health Insights 8:49–59
    [Google Scholar]
  43. 43. 
    Klotz SA, Dorn PL, Klotz JH, Pinnas JL, Weirauch C et al. 2009. Feeding behavior of triatomines from the southwestern United States: an update on potential risk for transmission of Chagas disease. Acta Trop 111:114–18
    [Google Scholar]
  44. 44. 
    Zeledon R, Alvarado R, Jiron LF. 1977. Observations on the feeding and defecation patterns of three triatomine species (Hemiptera: Reduviidae). Acta Trop 34:65–77
    [Google Scholar]
  45. 45. 
    Reisenman CE, Gregory T, Guerenstein PG, Hildebrand JG. 2011. Feeding and defecation behavior of Triatoma rubida (Uhler, 1894) (Hemiptera: Reduviidae) under laboratory conditions, and its potential role as a vector of Chagas disease in Arizona, USA. Am. J. Trop. Med. Hyg. 85:648–56
    [Google Scholar]
  46. 46. 
    Nouvellet P, Dumonteil E, Gourbiere S 2013. The improbable transmission of Trypanosoma cruzi to human: the missing link in the dynamics and control of Chagas disease. PLOS Negl. Trop. Dis. 7:e2505
    [Google Scholar]
  47. 47. 
    Kierszenbaum F, Gottlieb CA, Budzko DB. 1981. Antibody-independent, natural resistance of birds to Trypanosoma cruzi infection. J. Parasitol. 67:656–60
    [Google Scholar]
  48. 48. 
    Garrido R, Campos-Soto R, Quiroga N, Botto-Mahan C. 2020. Bloodmeal-stealing in wild-caught Mepraia spinolai (Hemiptera: Reduviidae), a sylvatic vector of Trypanosoma cruzi. Ecol. Entomol. 46:681–83
    [Google Scholar]
  49. 49. 
    Díaz-Albiter HM, Ferreira TN, Costa SG, Rivas GB, Gumiel M et al. 2016. Everybody loves sugar: first report of plant feeding in triatomines. Parasit. Vectors 9:114
    [Google Scholar]
  50. 50. 
    Duran P, Sinani E, Depickere S. 2016. On triatomines, cockroaches and haemolymphagy under laboratory conditions: new discoveries. Mem. Inst. Oswaldo Cruz 111:605–13
    [Google Scholar]
  51. 51. 
    Gürtler RE, Cardinal MV. 2015. Reservoir host competence and the role of domestic and commensal hosts in the transmission of Trypanosoma cruzi. Acta Trop 151:32–50
    [Google Scholar]
  52. 52. 
    Jaimes-Dueñez J, Triana-Chávez O, Cantillo-Barraza O, Hernández C, Ramírez JD, Góngora-Orjuela A. 2017. Molecular and serological detection of Trypanosoma cruzi in dogs (Canis lupus familiaris) suggests potential transmission risk in areas of recent acute Chagas disease outbreaks in Colombia. Prev. Vet. Med. 141:1–6
    [Google Scholar]
  53. 53. 
    Estrada-Franco JG, Bhatia V, Diaz-Albiter H, Ochoa-Garcia L, Barbabosa A et al. 2006. Human Trypanosoma cruzi infection and seropositivity in dogs, Mexico. Emerg. Infect. Dis. 12:624–30
    [Google Scholar]
  54. 54. 
    Vitt JP, Saunders AB, O'Brien MT, Mansell J, Ajithdoss DK, Hamer SA. 2016. Diagnostic features of acute Chagas myocarditis with sudden death in a family of boxer dogs. J. Vet. Intern. Med. 30:1210–15
    [Google Scholar]
  55. 55. 
    Kjos SA, Snowden KF, Craig TM, Lewis B, Ronald N, Olson JK 2008. Distribution and characterization of canine Chagas disease in Texas. Vet. Parasitol. 152:249–56
    [Google Scholar]
  56. 56. 
    Saunders AB, Hamer SA. 2020. Chagas disease: Trypanosoma cruzi infection in dogs. Today's Veterinary Practice July/Aug. 2–8 https://todaysveterinarypractice.com/chagas-disease-dogs/
    [Google Scholar]
  57. 57. 
    Gunter SM, Brown EL, Gorchakov R, Murray KO, Garcia MN 2017. Sylvatic transmission of Trypanosoma cruzi among domestic and wildlife reservoirs in Texas, USA: a review of the historical literature. Zoonoses Public Health 64:313–27
    [Google Scholar]
  58. 58. 
    Gunter SM, Cordray C, Gorchakov R, Du I, Dittmar B et al. 2018. Identification of white-tailed deer (Odocoileus virginianus) as a novel reservoir species for Trypanosoma cruzi in Texas, USA. J. Wildl. Dis. 54:814–18
    [Google Scholar]
  59. 59. 
    Zecca IB, Hodo CL, Swarts HM, DeMaar TW, Snowden KF et al. 2021. Trypanosoma cruzi and incidental Sarcocystis spp. in endangered ocelots (Leopardus pardalis) of South Texas, USA. J. Wildl. Dis. 57:667–71
    [Google Scholar]
  60. 60. 
    Ghersi BM, Peterson AC, Gibson NL, Dash A, Elmayan A et al. 2020. In the heart of the city: Trypanosoma cruzi infection prevalence in rodents across New Orleans. Parasites Vectors 13:577
    [Google Scholar]
  61. 61. 
    Hodo CL, Bañuelos RM, Edwards EE, Wozniak EJ, Hamer SA. 2020. Pathology and discrete typing unit associations of Trypanosoma cruzi infection in coyotes (Canis latrans) and raccoons (Procyon lotor) of Texas, USA. J. Wildl. Dis. 56:134–44
    [Google Scholar]
  62. 62. 
    Zecca IB, Hodo CL, Slack S, Auckland L, Hamer SA 2020. Trypanosoma cruzi infections and associated pathology in urban-dwelling Virginia opossums (Didelphis virginiana). Int. J. Parasitol. Parasites Wildl. 11:287–93
    [Google Scholar]
  63. 63. 
    Curtis-Robles R, Lewis BC, Hamer SA 2016. High Trypanosoma cruzi infection prevalence associated with minimal cardiac pathology among wild carnivores in central Texas. Int. J. Parasitol. Parasites Wildl. 5:117–23
    [Google Scholar]
  64. 64. 
    Rodriguez F, Luna BS, Calderon O, Manriquez-Roman C, Amezcua-Winter K et al. 2021. Surveillance of Trypanosoma cruzi infection in triatomine vectors, feral dogs and cats, and wild animals in and around El Paso county, Texas, and New Mexico. PLOS Negl. Trop. Dis. 15:e0009147
    [Google Scholar]
  65. 65. 
    Elmayan A, Tu W, Duhon B, Marx P, Wolfson W et al. 2019. High prevalence of Trypanosoma cruzi infection in shelter dogs from southern Louisiana, USA. Parasites Vectors 12:322
    [Google Scholar]
  66. 66. 
    Bradley KK, Bergman DK, Woods JP, Crutcher JM, Kirchhoff LV. 2000. Prevalence of American trypanosomiasis (Chagas disease) among dogs in Oklahoma. J. Am. Vet. Med. Assoc. 217:1853–57
    [Google Scholar]
  67. 67. 
    Beard CB, Pye G, Steurer FJ, Rodriguez R, Campman R et al. 2003. Chagas disease in a domestic transmission cycle, southern Texas, USA. Emerg. Infect. Dis. 9:103–5
    [Google Scholar]
  68. 68. 
    Hodo CL, Rodriguez JY, Curtis-Robles R, Zecca IB, Snowden KF et al. 2019. Repeated cross-sectional study of Trypanosoma cruzi in shelter dogs in Texas, in the context of Dirofilaria immitis and tick-borne pathogen prevalence. J. Vet. Intern. Med. 33:158–66
    [Google Scholar]
  69. 69. 
    Curtis-Robles R, Zecca IB, Roman-Cruz V, Carbajal ES, Auckland LD et al. 2017. Trypanosoma cruzi (agent of Chagas disease) in sympatric human and dog populations in “Colonias” of the Lower Rio Grande Valley of Texas. Am. J. Trop. Med. Hyg. 96:805–14
    [Google Scholar]
  70. 70. 
    Nieto PD, Boughton R, Dorn PL, Steurer F, Raychaudhuri S et al. 2009. Comparison of two immunochromatographic assays and the indirect immunofluorescence antibody test for diagnosis of Trypanosoma cruzi infection in dogs in south central Louisiana. Vet. Parasitol. 165:241–47
    [Google Scholar]
  71. 71. 
    Meyers AC, Meinders M, Hamer SA. 2017. Widespread Trypanosoma cruzi infection in government working dogs along the Texas-Mexico border: discordant serology, parasite genotyping and associated vectors. PLOS Negl. Trop. Dis. 11:e0005819
    [Google Scholar]
  72. 72. 
    Curtis-Robles R, Snowden KF, Dominguez B, Dinges L, Rodgers S et al. 2017. Epidemiology and molecular typing of Trypanosoma cruzi in naturally-infected hound dogs and associated triatomine vectors in Texas, USA. PLOS Negl. Trop. Dis. 11:e0005298
    [Google Scholar]
  73. 73. 
    Tenney TD, Curtis-Robles R, Snowden KF, Hamer SA 2014. Shelter dogs as sentinels for Trypanosoma cruzi transmission across Texas. Emerg. Infect. Dis. 20:1323–26
    [Google Scholar]
  74. 74. 
    Meyers AC, Hamer SA, Matthews D, Gordon SG, Saunders AB 2019. Risk factors and select cardiac characteristics in dogs naturally infected with Trypanosoma cruzi presenting to a teaching hospital in Texas. J. Vet. Intern. Med. 33:1695–706
    [Google Scholar]
  75. 75. 
    Burkholder JE, Allison TC, Kelly VP 1980. Trypanosoma cruzi (Chagas) (Protozoa: Kinetoplastida) in invertebrate, reservoir, and human hosts of the lower Rio Grande valley of Texas. J. Parasitol. 66:305–11
    [Google Scholar]
  76. 76. 
    Meyers AC, Edwards EE, Sanders JP, Saunders AB, Hamer SA. 2021. Fatal Chagas myocarditis in government working dogs in the southern United States: cross-reactivity and differential diagnoses in five cases across six months. Vet. Parasitol. 24:100545
    [Google Scholar]
  77. 77. 
    Meyers AC, Purnell JC, Ellis MM, Auckland LD, Meinders M, Hamer SA 2020. Nationwide exposure of U.S. working dogs to the Chagas disease parasite, Trypanosoma cruzi. Am. J. Trop. Med. Hyg. 102:1078–85
    [Google Scholar]
  78. 78. 
    Zecca IB, Hodo CL, Slack S, Auckland L, Rodgers S et al. 2020. Prevalence of Trypanosoma cruzi infection and associated histologic findings in domestic cats (Felis catus). Vet. Parasitol. 278:109014
    [Google Scholar]
  79. 79. 
    Gürtler RE, Cecere MC, Lauricella MA, Cardinal MV, Kitron U, Cohen JE 2007. Domestic dogs and cats as sources of Trypanosoma cruzi infection in rural northwestern Argentina. Parasitology 134:69–82
    [Google Scholar]
  80. 80. 
    Reis FC, Minuzzi-Souza TTC, Neiva M, Timbó RV, de Morais IOB et al. 2019. Trypanosomatid infections in captive wild mammals and potential vectors at the Brasilia Zoo, Federal District, Brazil. Vet. Med. Sci. 6:248–56
    [Google Scholar]
  81. 81. 
    Jaime-Andrade J, Avila-Figueroa D, Lozano-Kasten FJ, Hernández-Gutiérrez RJ, Magallón-Gastélum E et al. 1997. Acute Chagas' cardiopathy in a polar bear (Ursus maritimus) in Guadalajara, Mexico. Rev. Soc. Bras. Med. Trop. 30:337–40
    [Google Scholar]
  82. 82. 
    Huckins GL, Eshar D, Schwartz D, Morton M, Herrin BH et al. 2019. Trypanosoma cruzi infection in a zoo-housed red panda in Kansas. J. Vet. Diagn. Investig. 31:752–55
    [Google Scholar]
  83. 83. 
    Diaz-Delgado J, Kellerman TE, Auckland L, Ferro PJ, Groch KR et al. 2020. Trypanosoma cruzi genotype I and Toxoplasma gondii co-infection in a red-necked wallaby. J. Comp. Pathol. 179:52–58
    [Google Scholar]
  84. 84. 
    Osborn SD, Dalton LM, Behin P, Curtis-Robles R, Hamer SA et al. 2015. Diagnosis of Trypanosoma cruzi infection (Chagas disease) in a Pacific walrus (Odobenus rosmarus divergens). Case rep. Int. Assoc. Aquatic Anim. Med., Davis, CA. https://www.vin.com/apputil/content/defaultadv1.aspx?id=6651373&pid=12676&
  85. 85. 
    Weidner B, Sim RR, Hamer S, McCain S. 2019. Diagnosis and treatment of Chagas disease (Trypanosoma cruzi) in a naturally infected De Brazza's monkey (Cercopithecus neglectus) in Alabama Presented at the 51st Annual Meeting of the American Association of Zoo Veterinarians St. Louis, MO: Sept. 28–Oct. 4
    [Google Scholar]
  86. 86. 
    Grieves JL, Hubbard GB, Williams JT, Vandeberg JL, Dick EJ Jr. et al. 2008. Trypanosoma cruzi in non-human primates with a history of stillbirths: a retrospective study (Papio hamadryas spp.) and case report (Macaca fascicularis). J. Med. Primatol. 37:318–28
    [Google Scholar]
  87. 87. 
    Dorn PL, Daigle ME, Combe CL, Tate AH, Stevens L, Phillippi-Falkenstein KM. 2012. Low prevalence of Chagas parasite infection in a nonhuman primate colony in Louisiana. J. Am. Assoc. Lab. Anim. Sci. 51:443–47
    [Google Scholar]
  88. 88. 
    Hodo CL, Wilkerson GK, Birkner EC, Gray SB, Hamer SA. 2018. Trypanosoma cruzi transmission among captive nonhuman primates, wildlife, and vectors. Ecohealth 15:426–36
    [Google Scholar]
  89. 89. 
    Balouz V, Agüero F, Buscaglia CA. 2017. Chagas disease diagnostic applications: present knowledge and future steps. Adv. Parasitol. 97:1–45
    [Google Scholar]
  90. 90. 
    World Health Organ 2012. Research priorities for Chagas disease, human African trypanosomiasis and leishmaniasis Tech. Rep. 975 World Health Organ. Geneva:
    [Google Scholar]
  91. 91. 
    Kjos SA, Gillespie JJ, Olson JK, Snowden KF. 2009. Detection of Blastocrithidia spp. (Kinetoplastida: Trypanosomatidae) in Chagas disease vectors from Texas, USA. Vector Borne Zoonotic Dis. 9:213–16
    [Google Scholar]
  92. 92. 
    Cura CI, Duffy T, Lucero RH, Bisio M, Peneau J et al. 2015. Multiplex real-time PCR assay using TaqMan probes for the identification of Trypanosoma cruzi DTUs in biological and clinical samples. PLOS Negl. Trop. Dis. 9:e0003765
    [Google Scholar]
  93. 93. 
    Piron M, Fisa R, Casamitjana N, López-Chejade P, Puig L et al. 2007. Development of a real-time PCR assay for Trypanosoma cruzi detection in blood samples. Acta Trop. 103:195–200
    [Google Scholar]
  94. 94. 
    Pronovost H, Peterson AC, Chavez BG, Blum MJ, Dumonteil E, Herrera CP 2018. Deep sequencing reveals multiclonality and new discrete typing units of Trypanosoma cruzi in rodents from the southern United States. J. Microbiol. Immunol. Infect. 53:622–33
    [Google Scholar]
  95. 95. 
    Yabsley MJ, Brown EL, Roellig DM. 2009. Evaluation of the Chagas Stat-Pak assay for detection of Trypanosoma cruzi antibodies in wildlife reservoirs. J. Parasitol. 95:775–77
    [Google Scholar]
  96. 96. 
    Borland EM, Kading RC. 2021. Modernizing the toolkit for arthropod bloodmeal identification. Insects 12:37
    [Google Scholar]
  97. 97. 
    Antonio-Campos A, Alejandre-Aguilar R, Rivas N. 2020. Unraveling the importance of triatomine (Hemiptera: Reduviidae: Triatominae) feeding sources in the Chagas disease context. Ann. Entomol. Soc. Am. 114:48–58
    [Google Scholar]
  98. 98. 
    Ocaña-Mayorga S, Bustillos JJ, Villacís AG, Pinto CM, Brenière SF Grijalva MJ. 2021. Triatomine feeding profiles and Trypanosoma cruzi infection, implications in domestic and sylvatic transmission cycles in Ecuador. Pathogens 10:42
    [Google Scholar]
  99. 99. 
    Bezerra CM, Barbosa SE, Souza RCM, Barezani CP, Gürtler RE et al. 2018. Triatoma brasiliensis Neiva, 1911: food sources and diversity of Trypanosoma cruzi in wild and artificial environments of the semiarid region of Ceara, northeastern Brazil. Parasites Vectors 11:642
    [Google Scholar]
  100. 100. 
    Gottdenker NL, Chaves LF, Calzada JE, Saldana A, Carroll CR. 2012. Host life history strategy, species diversity, and habitat influence Trypanosoma cruzi vector infection in changing landscapes. PLOS Negl. Trop. Dis. 6:e1884
    [Google Scholar]
  101. 101. 
    Arias-Giraldo LM, Muñoz M, Hernández C, Herrera G, Velásquez-Ortiz N et al. 2020. Identification of blood-feeding sources in Panstrongylus, Psammolestes, Rhodnius and Triatoma using amplicon-based next-generation sequencing. Parasites Vectors 13:434
    [Google Scholar]
  102. 102. 
    Dumonteil E, Ramirez-Sierra MJ, Pérez-Carrillo S, Teh-Poot C, Herrera C et al. 2018. Detailed ecological associations of triatomines revealed by metabarcoding and next-generation sequencing: implications for triatomine behavior and Trypanosoma cruzi transmission cycles. Sci. Rep. 8:4140
    [Google Scholar]
  103. 103. 
    Kieran TJ, Gottdenker NL, Varian CP, Saldaña A, Means N et al. 2017. Blood meal source characterization using Illumina sequencing in the Chagas disease vector Rhodnius pallescens (Hemiptera: Reduviidae) in Panama. J. Med. Entomol. 54:1786–89
    [Google Scholar]
  104. 104. 
    Keller JI, Lima-Cordon R, Monroy MC, Schmoker AM, Zhang F et al. 2019. Protein mass spectrometry detects multiple bloodmeals for enhanced Chagas disease vector ecology. Infect. Genet. Evol. 74:103998
    [Google Scholar]
  105. 105. 
    Curtis-Robles R, Meyers AC, Auckland LD, Zecca IB, Skiles R, Hamer SA. 2018. Parasitic interactions among Trypanosoma cruzi, triatomine vectors, domestic animals, and wildlife in Big Bend National Park along the Texas-Mexico border. Acta Trop 188:225–33
    [Google Scholar]
  106. 106. 
    Dye-Braumuller KC, Gorchakov R, Gunter SM, Nielsen DH, Roachell WD et al. 2019. Identification of triatomines and their habitats in a highly developed urban environment. Vector Borne Zoonotic Dis. 19:265–73
    [Google Scholar]
  107. 107. 
    Garcia MN, Aguilar D, Gorchakov R, Rossmann SN, Montgomery SP et al. 2015. Evidence of autochthonous Chagas disease in southeastern Texas. Am. J. Trop. Med. Hyg. 92:325–30
    [Google Scholar]
  108. 108. 
    Gorchakov R, Trosclair LP, Wozniak EJ, Feria PT, Garcia MN et al. 2016. Trypanosoma cruzi infection prevalence and bloodmeal analysis in triatomine vectors of Chagas disease from rural peridomestic locations in Texas, 2013–2014. J. Med. Entomol. 53:911–18
    [Google Scholar]
  109. 109. 
    Kjos SA, Marcet PL, Yabsley MJ, Kitron U, Snowden KF et al. 2013. Identification of bloodmeal sources and Trypanosoma cruzi infection in triatomine bugs (Hemiptera: Reduviidae) from residential settings in Texas, the United States. J. Med. Entomol. 50:1126–39
    [Google Scholar]
  110. 110. 
    Klotz SA, Schmidt JO, Dorn PL, Ivanyi C, Sullivan KR, Stevens L. 2014. Free-roaming kissing bugs, vectors of Chagas disease, feed often on humans in the Southwest. Am. J. Med. 127:421–26
    [Google Scholar]
  111. 111. 
    Stevens L, Dorn PL, Hobson J, de la Rua NM, Lucero DE et al. 2012. Vector blood meals and Chagas disease transmission potential, United States. Emerg. Infect. Dis. 18:646–49
    [Google Scholar]
  112. 112. 
    Waleckx E, Suarez J, Richards B, Dorn PL. 2014. Triatoma sanguisuga blood meals and potential for Chagas disease, Louisiana, USA. Emerg. Infect. Dis. 20:2141–43
    [Google Scholar]
  113. 113. 
    Dormann CF, Fründ J, Gruber B. 2008. Introducing the bipartite package: analysing ecological networks. R News 8:8–11
    [Google Scholar]
  114. 114. 
    Bivona AE, Alberti AS, Cerny N, Trinitario SN, Malchiodi EL. 2020. Chagas disease vaccine design: the search for an efficient Trypanosoma cruzi immune-mediated control. Biochim. Biophys. Acta Mol. Basis Dis. 1866:165658
    [Google Scholar]
  115. 115. 
    Quijano-Hernandez I, Dumonteil E. 2011. Advances and challenges towards a vaccine against Chagas disease. Hum. Vaccines 7:1184–91
    [Google Scholar]
  116. 116. 
    Rodríguez-Morales O, Pérez-Leyva MM, Ballinas-Verdugo MA, Carrillo-Sánchez SC, Rosales-Encina JL et al. 2012. Plasmid DNA immunization with Trypanosoma cruzi genes induces cardiac and clinical protection against Chagas disease in the canine model. Vet. Res. 43:79
    [Google Scholar]
  117. 117. 
    Aparicio-Burgos JE, Zepeda-Escobar JA, de Oca-Jimenez RM, Estrada-Franco JG, Barbabosa-Pliego A et al. 2015. Immune protection against Trypanosoma cruzi induced by TcVac4 in a canine model. PLOS Negl. Trop. Dis. 9:e0003625
    [Google Scholar]
  118. 118. 
    Meymandi S, Hernandez S, Park S, Sanchez DR, Forsyth C. 2018. Treatment of Chagas disease in the United States. Curr. Treat. Options Infect. Dis. 10:373–88
    [Google Scholar]
  119. 119. 
    Zao C-L, Yang Y-C, Tomanek L, Cooke A, Berger R et al. 2019. PCR monitoring of parasitemia during drug treatment for canine Chagas disease. J. Vet. Diagn. Investig. 31:742–46
    [Google Scholar]
  120. 120. 
    Madigan R, Majoy S, Ritter K, Concepción JL, Márquez ME et al. 2019. Investigation of a combination of amiodarone and itraconazole for treatment of American trypanosomiasis (Chagas disease) in dogs. JAVMA 255:317–29
    [Google Scholar]
  121. 121. 
    Castro LA, Peterson JK, Saldana A, Perea MY, Calzada JE et al. 2014. Flight behavior and performance of Rhodnius pallescens (Hemiptera: Reduviidae) on a tethered flight mill. J. Med. Entomol. 51:1010–18
    [Google Scholar]
  122. 122. 
    Lazzari CR, Pereira MH, Lorenzo MG. 2013. Behavioural biology of Chagas disease vectors. Mem. Inst. Oswaldo Cruz 108:Suppl. 134–47
    [Google Scholar]
  123. 123. 
    Barrozo RB, Reisenman CE, Guerenstein P, Lazzari CR, Lorenzo MG. 2017. An inside look at the sensory biology of triatomines. J. Insect Physiol. 97:3–19
    [Google Scholar]
  124. 124. 
    Indacochea A, Gard CC, Hansen IA, Pierce J, Romero A. 2017. Short-range responses of the kissing bug Triatoma rubida (Hemiptera: Reduviidae) to carbon dioxide, moisture, and artificial light. Insects 8:90
    [Google Scholar]
  125. 125. 
    Pacheco-Tucuch FS, Ramirez-Sierra MJ, Gourbière S, Dumonteil E 2012. Public street lights increase house infestation by the Chagas disease vector Triatoma dimidiata. PLOS ONE 7:4e36207
    [Google Scholar]
  126. 126. 
    Nieto-Sanchez C, Bates BR, Guerrero D, Jimenez S, Baus EG et al. 2019. Home improvement and system-based health promotion for sustainable prevention of Chagas disease: a qualitative study. PLOS Negl. Trop. Dis. 13:e0007472
    [Google Scholar]
  127. 127. 
    Gürtler RE, Kitron U, Cecere MC, Segura EL, Cohen JE. 2007. Sustainable vector control and management of Chagas disease in the Gran Chaco, Argentina. PNAS 104:16194–99
    [Google Scholar]
  128. 128. 
    Cecere MC, Vasquez-Prokopec GM, Gürtler RE, Kitron U. 2006. Reinfestation sources for Chagas disease vector. Triatoma infestans, Argentina. Emerg. Infect. Dis. 12:1096–102
    [Google Scholar]
  129. 129. 
    Loza A, Talaga A, Herbas G, Canaviri RJ, Cahuasiri T et al. 2017. Systemic insecticide treatment of the canine reservoir of Trypanosoma cruzi induces high levels of lethality in Triatoma infestans, a principal vector of Chagas disease. Parasites Vectors 10:344
    [Google Scholar]
  130. 130. 
    Laiño MA, Cardinal MV, Enriquez GF, Alvedro A, Gaspe MS, Gürtler RE. 2019. An oral dose of Fluralaner administered to dogs kills pyrethroid-resistant and susceptible Chagas disease vectors for at least four months. Vet. Parasitol. 268:98–104
    [Google Scholar]
  131. 131. 
    Queiroga TBD, Gomez LCP, de Sena ER, Dos Santos WV, Ferreira HRP, de Araújo-Neto VT 2021. Insecticidal efficacy of fluralaner (Bravecto®) against Triatoma brasiliensis, a major vector of Trypanosoma cruzi in Brazil. Parasites Vectors 14:456
    [Google Scholar]
  132. 132. 
    Hurwitz I, Fieck A, Klein N, Jose C, Kang A, Durvasula RV 2011. A paratransgenic strategy for the control of Chagas disease. Psyche 2012:178930
    [Google Scholar]
  133. 133. 
    Beard CB, Cordon-Rosales C, Durvasula RV. 2002. Bacterial symbionts of the Triatominae and their potential use in control of Chagas disease transmission. Annu. Rev. Entomol. 47:123–41
    [Google Scholar]
  134. 134. 
    Durvasula RV, Kroger A, Goodwin M, Panackal A, Kruglov O et al. 1999. Strategy for introduction of foreign genes into field populations of Chagas disease vectors. Ann. Entomol. Soc. Am. 92:937–43
    [Google Scholar]
  135. 135. 
    Taracena ML, Oliveira PL, Almendares O, Umana C, Lowenberger C et al. 2015. Genetically modifying the insect gut microbiota to control Chagas disease vectors through systemic RNAi. PLOS Negl. Trop. Dis. 9:e0003358
    [Google Scholar]
  136. 136. 
    López JDS, Monroy MC, Dorn PL, Castellanos S, Lima R, Rodas A. 2019. Effect of community education in an integrate control for Triatoma dimidiata (Hemitpera: Reduviidae). Rev. Cuba. Med. Trop. 71:380
    [Google Scholar]
  137. 137. 
    Gürtler RE, Yadon ZE. 2015. Eco-bio-social research on community-based approaches for Chagas disease vector control in Latin America. Trans. R. Soc. Trop. Med. Hyg. 109:91–98
    [Google Scholar]
  138. 138. 
    Patterson NM, Bates BR, Chadwick AE, Neito-Sanchez C, Grijalva MJ. 2018. Using the health belief model to identify communication opportunities to prevent Chagas disease in Southern Ecuador. PLOS Negl. Trop. Dis. 12:e0006841
    [Google Scholar]
  139. 139. 
    Curtis-Robles R, Wozniak EJ, Auckland LD, Hamer GL, Hamer SA. 2015. Combining public health education and disease ecology research: using citizen science to assess Chagas disease entomological risk in Texas. PLOS Negl. Trop. Dis. 9:e0004235
    [Google Scholar]
  140. 140. 
    Gibbs EP. 2014. The evolution of One Health: a decade of progress and challenges for the future. Vet. Rec. 174:85–91
    [Google Scholar]
  141. 141. 
    Bonney CH, Schmidt RE. 1975. A mixed infection: Chagas’ and Tyzzer's disease in a lesser panda. J. Zoo Anim. Med. 6:4–7
    [Google Scholar]
  142. 142. 
    Hall CA, Polizzi C, Yabsley MJ, Norton TM. 2007. Trypanosoma cruzi prevalence and epidemiologic trends in lemurs on St. Catherines Island, Georgia. J. Parasitol. 93:93–96
    [Google Scholar]
  143. 143. 
    Pung OJ, Spratt J, Clark CG, Norton TM, Carter J 1998. Trypanosoma cruzi infection of free-ranging lion-tailed macaques (Macaca silenus) and ring-tailed lemurs (Lemur catta) on St. Catherine's Island, Georgia, USA. J. Zoo Wildl. Med. 29:25–30
    [Google Scholar]
  144. 144. 
    Latas PJ, Reavill D. 2019. Trypanosoma cruzi infection in sugar gliders (Petaurus breviceps) and hedgehogs (Atelerix albiventris) via ingestion. J. Exot. Pet. Med. 29:76–78
    [Google Scholar]
  145. 145. 
    Fletcher KC, Hubbard GB. 1985. Fatal cardiomyopathy caused by Trypanosoma cruzi in an aardwolf. J. Am. Vet. Med. Assoc. 187:1263–64
    [Google Scholar]
  146. 146. 
    Olson LC, Skinner SF, Palotay JL, McGhee GE. 1986. Encephalitis associated with Trypanosoma cruzi in a Celebes black macaque. Lab. Anim. Sci. 36:667–70
    [Google Scholar]
  147. 147. 
    Šafářová B, Giusti CH, Perez MP, Zecca IB, Carbajal ES et al. 2021. Habitat and environmental risks of Chagas disease in low-income colonias and peri-urban subdivisions in South Texas. Habitat Int. 118:102460
    [Google Scholar]
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