Clinicopathological alterations in wild mammals from the reservoir system of Trypanosoma cruzi: a scoping review

Ricardo Sánchez Pérez1()(), José Manuel Aranda-Coello2()(), José Antonio De Fuentes Vicente3()(), Oscar Rico Chávez4()()

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Animal Disease ›› 2024, Vol. 4 ›› Issue (1) : 6. DOI: 10.1186/s44149-024-00111-4

Clinicopathological alterations in wild mammals from the reservoir system of Trypanosoma cruzi: a scoping review

  • Ricardo Sánchez Pérez1()(), José Manuel Aranda-Coello2()(), José Antonio De Fuentes Vicente3()(), Oscar Rico Chávez4()()
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Abstract

Trypanosoma cruziis the etiologic agent of Chagas disease. This flagellated protozoan is transmitted to humans as well as different species of domestic and wild animals viavectors from the Reduviidae family (known as “kissing bugs”). Despite the fact that hundreds of species of wild mammals are part of the reservoir system, the morphological changes and clinical manifestations resulting from the pathogenesis of the infection have been largely neglected. The aim of this review is to systematically compile the available information regarding clinicopathological alterations in wild mammals due to natural infection by T. cruzi. Information was obtained from six online bibliographic data search platforms, resulting in the identification of 29 publications that met the inclusion criteria. Mortality was the most common clinical manifestation, cardiac damage was the main finding at necropsy, and lymphoplasmacytic inflammation was the most frequent microscopic injury. Thus, regardless of its role as a reservoir, T. cruzihas the potential to affect the health status of wild mammals, a situation that highlights the need for further research to analyze, measure, and compare its effects at both the individual and population levels.

Keywords

Trypanosoma cruzi / Chagas disease / American trypanosomiasis / Clinicopathological alterations / Natural infection / Wild mammals

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Ricardo Sánchez Pérez, José Manuel Aranda-Coello, José Antonio De Fuentes Vicente, Oscar Rico Chávez. Clinicopathological alterations in wild mammals from the reservoir system of Trypanosoma cruzi: a scoping review. Animal Disease, 2024, 4(1): 6 https://doi.org/10.1186/s44149-024-00111-4

References

[1]
Andrade, M.C.R., E.J. Dick Jr., R. Guardado-Mendoza, M.L. Hohmann, D.C.P. Mejido, J.L. VandeBerg, C.D. DiCarlo, and G.B. Hubbard. 2009. Nonspecific lymphocytic myocarditis in baboons is associated with Trypanosoma cruzi infection. The American Journal of Tropical Medicine and Hygiene 81 (2): 235. https://doi.org/10.4269/ajtmh.2009.81.235.
[2]
Araujo Carreira, J.C., A.M. Jansen, M.P. Deane, and H.L. Lenzi. 1996. Histopathological study of experimental and natural infections by Trypanosoma cruzi in Didelphis marsupialis. Memorias Do Instituto Oswaldo Cruz 91 (5): 609–618. https://doi.org/10.1590/s0074-02761996000500012.
[3]
Arksey, Hilary, and Lisa O’Malley. 2005. Scoping studies: Toward a methodological framework. International Journal of Social Research Methodology: Theory and Practice 8 (1): 19–32. https://doi.org/10.1080/1364557032000119616.
[4]
Badra, E.S., M.A. Sala, R.A. Lopes, J.C. Prado, S. Albuquerque, S. Zucoloto, and A.A. Carraro-Abrah?o. 2008. Histopathological changes in the placentas and fetuses of mice infected with Trypanosoma cruzi Isolated from the Myotis nigricans nigricans bat. Journal of Comparative Pathology 139 (2–3): 108–112. https://doi.org/10.1016/j.jcpa.2008.05.009.
[5]
Barr, Stephen C., and Dwight D. Bowman. 2012. Blackwell’s five-minute veterinary consult clinical companion canine and feline infectious diseases and parasitology, 2nd ed. Oxford: Wiley – Blackwell. ISBN-10: 081382012
[6]
Barr, S.C., C.C. Brown, V.A. Dennis, and T.R. Klei. 1991. The lesions and prevalence of Trypanosoma cruzi in opossums and armadillos from southern Louisiana. Journal of Parasitology 77 (4): 624–627. https://doi.org/10.2307/3283170.
[7]
Barros, F.D.N.L., F.D. Sampaio Júnior, S.D.M. Costa, D.M.D. Farias, M.A.O. Moura, P.S. Bezerra Júnior, G. Góes-Cavalcante, and A. Scofield. 2020. First report of natural infection by Trypanosoma cruzi in secretions of the scent glands and myocardium of Philander opossum (Marsupialia: Didelphidae): Parasitological and clinicopathological findings. Veterinary Parasitology: Regional Studies and Reports 22: 100463. https://doi.org/10.1016/j.vprsr.2020.100463.
[8]
Beugnet, Frédéric, and Léna?g. Halos. 2018. Textbook of clinical parasitology in dogs and cats, 1st ed. Zaragoza: Servet. ISBN: 2955080527
[9]
Bommineni, Y.R., E.J. Dick, J.S. Estep, J.L. Van de Berg, and G.B. Hubbard. 2009. Fatal acute Chagas disease in a chimpanzee. Journal of Medical Primatology 38 (4): 247–251. https://doi.org/10.1111/J.1600-0684.2009.00348.X.
[10]
Bramer, Wichor M., Gerdien B. de Jonge, Melissa L. Rethlefsen, Frans Mast, and Jos Kleijnen. 2018. A systematic approach to searching: An efficient and complete method to develop literature searches. Journal of the Medical Library Association 106 (4): 531–541. https://doi.org/10.5195/jmla.2018.283.
[11]
Carnevali, V., B. Nogueda-Torres, M.E. Villagrán-Herrera, J.A. De Diego-Cabrera, G. Rocha-Chávez, and J.A. Martínez-Ibarra. 2017. Prevalence of Trypanosoma cruzi and organ alterations in Virginia opossums (Didelphis virginiana) from western Mexico–short communication. Acta Veterinaria Hungarica 65 (4): 505–509. https://doi.org/10.1556/004.2017.048.
[12]
Comeaux, J.M., R. Curtis-Robles, B.C. Lewis, K.J. Cummings, B.T. Mesenbrink, B.R. Leland, M.J. Bodenchuk, and S.A. Hamer. 2016. Survey of feral swine (Sus scrofa) infection with the agent of Chagas disease (Trypanosoma cruzi) in Texas, 2013–14. Journal of Wildlife Diseases 52 (3): 627–630. https://doi.org/10.7589/2015-08-208.
[13]
Coura, J.R., and A.C.V. Junqueira. 2015. Ecological diversity of Trypanosoma cruzi transmission in the Amazon basin. The main scenaries in the Brazilian Amazon. Acta Tropica 151 (1): 51–57. https://doi.org/10.1016/j.actatropica.2015.04.029.
[14]
Cruz-Reyes, Alejandro, and José Miguel Pickering-López. 2006. Chagas disease in Mexico: An analysis of geographical distribution during the past 76 years - a review. Memórias Do Instituto Oswaldo Cruz 101 (4): 345–354. https://doi.org/10.1590/S0074-02762006000400001.
[15]
Curtis-Robles, R., B.C. Lewis, and S.A. Hamer. 2016. High Trypanosoma cruzi infection prevalence associated with minimal cardiac pathology among wild carnivores in central Texas. International Journal for Parasitology: Parasites and Wildlife 5 (2): 117–123. https://doi.org/10.1016/j.ijppaw.2016.04.001.
[16]
Davis, D.S., L.H. Russell, L.G. Adams, R.G. Yaeger, and R.M. Robinson. 1980. An experimental infection of Trypanosoma cruzi in striped skunks (Mephitis Mephitis). Journal of Wildlife Diseases 16 (3): 403–406. https://doi.org/10.7589/0090-3558-16.3.403.
[17]
De Brito, T., and L.M. Deane. 1966. Aspectos anátomo-patológicos da infec??o natural de alguns animais silvestres pelo Trypanosoma cruzi. Revista Do Instituto De Medicina Tropical De S?o Paulo 8 (2): 79–82. https://doi.org/10.3389/fvets.2020.568745.
[18]
De Alba-Alvarado, Mariana, Martha Irene Bucio-Torres, Edgar Zenteno, Enrique Sampedro-Carrillo, Mariana Hernández-Lopez, Olivia Reynoso-Ducoing, Elia Torres-Gutiérrez, et al. 2020. Response to infection by Trypanosoma cruzi in a murine model. Frontiers in Veterinary Science 7: 1–11. https://doi.org/10.3389/fvets.2020.568745.
[19]
Desquesnes, M. 2017. Veterinary aspects. In American trypanosomiasis Chagas disease: One hundred years of research, 2nd edition, 283–98. Elsevier Inc. https://doi.org/10.1016/B978-0-12-801029-7.00013-7.
[20]
Díaz-Delgado, J., T.E. Kellerman, L. Auckland, P.J. Ferro, K.R. Groch, G. Gomez, and S.A. Hamer. 2020. Trypanosoma cruzi genotype I and Toxoplasma gondii coinfection in a red-necked wallaby. Journal of Comparative Pathology 179: 52–58. https://doi.org/10.2147/RRTM.S21683.
[21]
Fernandes, Maria Cecilia, and Norma W. Andrews. 2012. Host cell invasion by Trypanosoma cruzi: A unique strategy that promotes persistence. FEMS Microbiology Reviews 36 (3): 734–747. https://doi.org/10.1111/j.1574-6976.2012.00333.x.
[22]
González-Vieyra, Sandra Díaz, Ninfa Ramírez-Durán, ángel H. Sandoval-Trujillo, Juan Carlos Vazquez Chagoyan, and Alberto Barbabosa-Pliego. 2011. Trypanosoma cruzi in dogs: Electrocardiographic and echocardiographic evaluation, in Malinalco, State of Mexico. In Research and reports in tropical medicine, December, 155. https://doi.org/10.2147/rrtm.s21683.
[23]
Greene, Craigh E. 2012. Infectious diseases of the dog and cat, 4th ed. St. Louis: Elsevier.
[24]
Grieves, J.L., G.B. Hubbard, J.T. Williams, J.L. Vandeberg, E.J. Dick, J.C. López-Alvarenga, and N.E. Schlabritz-loutsevitch. 2008. Trypanosoma cruzi in nonhuman primates with a history of stillbirths: A retrospective study (Papio hamadryas spp.) and case report (Macaca fascicularis). Journal of Medical Primatology 37 (6): 318–328. https://doi.org/10.1111/J.1600-0684.2008.00302.
[25]
Gunn, Alan, and Sara J. Pitt. 2012. Parasitic Protozoa, Fungi and Plants. In Parasitology, an integrated approach, 1st ed., 28–85 Oxford: Wiley – Blackwell.
[26]
Hamer, Sarah, and Carolyn Hodo. 2019. Chagas disease: Wildlife infection with Trypanosoma cruzi in a one health context. In Fowler’s zoo and wild animal medicine current therapy, vol. 9, ed. Eric R. Miller and Murray E. Fowler, 239–46. St. Louis: Elsevier. https://doi.org/10.1016/B978-0-323-55228-8.00035-7.
[27]
Henderson, S.E., S.C. Pfeiffer, J. Novak, and T.A. Peace. 2020. Large granular lymphocytosis in a cynomolgus macaque (Macaca fascicularis) with a subclinical Trypanosoma cruzi infection. Veterinary Clinical Pathology 49 (3): 382–388. https://doi.org/10.1111/VCP.12879.
[28]
Hodo, Carolyn L., and Sarah A. Hamer. 2017. Toward an ecological framework for assessing reservoirs of vector-borne pathogens: Wildlife reservoirs of Trypanosoma cruzi across the southern United States. ILAR Journal 58 (3): 379–392. https://doi.org/10.1093/ilar/ilx020.
[29]
Hodo, C.L., R.M. Ba?uelos, E.E. Edwards, E.J. Wozniak, and S.A. Hamer. 2020. Pathology and discrete typing unit associations of Trypanosoma cruzi infection in coyotes (Canis latrans) and raccoons (Procyon lotor) of Texas, USA. Journal of Wildlife Diseases 56 (1): 134–144. https://doi.org/10.7589/2019-03-071.
[30]
Huckins, G.L., D. Eshar, D. Schwartz, M. Morton, B.H. Herrin, A. Cerezo, M.J. Yabsley, and S.M. Schneider. 2019. Trypanosoma cruzi infection in a zoo-housed red panda in Kansas. Journal of Veterinary Diagnostic Investigation 31 (5): 752–755. https://doi.org/10.1177/1040638719865926.
[31]
Jaime-Andrade, J., D. Avila-Figueroa, F.J. Lozano-Kasten, R.J. Hernández-Gutiérrez, E. Magallón-Gastélum, M.J. Kasten-Monges, and E.R. Lopes. 1997. Acute Chagas’ cardiopathy in a polar bear (Ursus maritimus) in Guadalajara, Mexico. Revista Da Sociedade Brasileira De Medicina Tropical 30 (4): 337–340. https://doi.org/10.1590/S0037-86821997000400011.
[32]
Jansen, A.M., S.C.C. Xavier, and A.L.R. Roque. 2017a. Ecological aspects of Trypanosoma cruzi: Wild hosts and reservoirs. In American trypanosomiasis Chagas disease: One hundred years of research: second edition, 243–259. Elsevier Inc. https://doi.org/10.1016/B978-0-12-801029-7.00011-3.
[33]
Jansen, A.M., S.C.C. Xavier, and A.L.R. Roque. 2017b. Trypanosoma cruzi enzootic cycle: General aspects, domestic and synanthropic hosts and reservoirs. In American trypanosomiasis Chagas disease: One hundred years of research: second edition, 265–78. Elsevier Inc. https://doi.org/10.1016/B978-0-12-801029-7.00012-5. https://www.sciencedirect.com/science/article/abs/pii/B9780128010297000125
[34]
Jansen, Ana Maria, Samanta Cristina Das Chagas Xavier, and André Luiz Rodrigues Roque. 2018. Trypanosoma cruzi transmission in the wild and its most important reservoir hosts in Brazil. Parasites and Vectors 11 (1). https://doi.org/10.1186/s13071-018-3067-2.
[35]
Latas, P.J., and D. Reavill. 2019. Trypanosoma cruzi infection in sugar gliders (Petaurus breviceps) and hedgehogs (Atelerix albiventris) via ingestion. Journal of Exotic Pet Medicine 29: 76–78. https://doi.org/10.1053/j.jepm.2018.10.007.
[36]
Legey, A.P., A.P. Pinho, S.C.C. Xavier, R. Marchevsky, J.C. Carreira, L.L. Leon, and A.M. Jansen. 2003. Trypanosoma cruzi in marsupial didelphids (Philander frenata and Didelhis marsupialis): Differences in the humoral immune response in natural and experimental infections. Revista Da Sociedade Brasileira De Medicina Tropical 36 (2): 241–248. https://doi.org/10.1590/s0037-86822003000200008.
[37]
Marinho, Claudio R.F., Daniella Z. Bucci, Lúcia Z. Maria, Karina R.B. Dagli, Marcos G. Bastos, Luiz R. Grisotto, Cristiane R.G.M. Sardinha, Carlos Penha Baptista, Maria Regina Gon?alves, D’Império Lima, et al. 2004. Pathology affects different organs in two mouse strains chronically infected by a Trypanosoma cruzi clone: A model for genetic studies of Chagas’ disease. Infection and Immunity 72 (4): 2350–2357. https://doi.org/10.1128/IAI.72.4.2350-2357.2004.
[38]
Martínez-Hernández, Fernando, Brizia Oria-Martínez, Emilio Rendón-Franco, Guiehdani Villalobos, and Claudia Irais Mu?oz-García. 2022. Trypanosoma cruzi, beyond the dogma of non-infection in birds. Infection, Genetics and Evolution 99: 1–7. https://doi.org/10.1016/j.meegid.2022.105239.
[39]
Mbaya, A.W., M.M. Aliyu, and U.I. Ibrahim. 2009. The clinico-pathology and mechanisms of trypanosomosis in captive and free-living wild animals: A review. Veterinary Research Communications 33: 793–809. https://doi.org/10.1007/s11259-009-9214-7.
[40]
Milei, J., O. Scoroo, M.A. Basombrio, R.L. Beigelman, and R.A. Storino. 1989. Myocardial involvement in Cavia porcellus naturally infected with Trypanosoma cruzi. Revista Medicina 49 (4): 315.
[41]
Moncayo, and A.C. Silveira. 2017. Current epidemiological trends of Chagas disease in Latin America and future challenges: Epidemiology, surveillance, and health policies. In American trypanosomiasis Chagas disease: One hundred years of research: second edition, 59–88. Elsevier Inc. https://doi.org/10.1016/B978-0-12-801029-7.00004-6.
[42]
Mubiru, J.N., A. Yang, E.J. Dick Jr., M. Owston, R.M. Sharp, J.F. VandeBerg, R.E. Shade, and J.L. VandeBerg. 2014. Correlation between presence of Trypanosoma cruzi DNA in heart tissue of baboons and cynomolgus monkeys, and lymphocytic myocarditis. The American Journal of Tropical Medicine and Hygiene 90 (4): 627. https://doi.org/10.4269/ajtmh.13-0448.
[43]
Pietrzak, S.M., and O.J. Pung. 1998. Trypanosomiasis in raccoons from Georgia. Journal of Wildlife Diseases 34 (1): 132–136. https://doi.org/10.7589/0090-3558-34.1.132.
[44]
Rodrigues Coura, Jose. 2007. Chagas disease: Whats is know and what is needed - A background article. Memórias Do Instituto Oswaldo Cruz 102 (1): 113–122. https://doi.org/10.1590/s0074-02762007000900018.
[45]
Rodrigues da Silva, Diana, Lisboa Lisboa de Castro, Monique Castro da Silva Alves, Wanderson da Silva Batista, and Gabriel Melo de Oliveira. 2016. Acute experimental Trypanosoma cruzi infection: Establishing a murine model that utilizes non-invasive measurements of disease parameters. Memorias Do Instituto Oswaldo Cruz 107 (2): 211–216. https://doi.org/10.1590/s0074-02762012000200010.
[46]
Rodrigues Roque, André Luiz, Paulo Sérgio D’Andrea, Gisele Braziliano De Andrade, and Ana Maria Jansen. 2005. Trypanosoma cruzi: Distinct patterns of infection in the sibling caviomorph rodent species Thrichomys apereoides laurentius and Thrichomys Pachyurus (Rodentia, Echimyidae). Experimental Parasitology 111 (1): 37–46. https://doi.org/10.1016/j.exppara.2005.05.003.
[47]
Rojo, Gemma, Francisca Pèlissier, Alejandra Sandoval-Rodriguez, Antonella Bacigalupo, Vanessa García, Raquel Pinto, Sylvia Ortiz, Carezza Botto-Mahan, Pedro E. Cattan, and Aldo Solari. 2020. Organs infected with Trypanosoma cruzi and DTU identification in the naturally, infected rodent Octodon degus. Experimental Parasitology 215: 107931. https://doi.org/10.1016/j.exppara.2020.107931.
[48]
Ryan, C.P., P.E. Hughes, and E.B. Howard. 1985. American trypanosomiasis (Chagas’ disease) in a striped skunk. Journal of Wildlife Diseases 21 (2): 175–176. https://doi.org/10.7589/0090-3558-21.2.175.
[49]
Salazar-Schettino, Paz María, Martha Irene Bucio-Torres, Margarita Cabrera-Bravo, Mariana Citlalli De Alba-Alvarado, Diana Rocío Castillo-Salda?a, Edgar Arturo Zenteno-Galindo, Julieta Rojo-Medina, Nadia Angélica Fernández-Santos, and Gabriela Perera-Salazar. 2016. Enfermedad de Chagas En México. Revista De La Facultad De Medicina De La UNAM 59 (3): 6–16. ISSN 2448-4865 Available in: http://ve.scielo.org/scielo.php?script=sci_arttext&pid=S169046482011000100010&lng=es&nrm=iso
[50]
Thompson, J.M., C.A. Habrun, C.M. Scully, E. Sasaki, R.W. Bauer, R. Jania, R.E. Baker, A.M. Chapman, A. Majeau, and H. Pronovost. 2021. Locally transmitted Trypanosoma cruzi in a domestic llama (Lama glama) in a rural area of Greater New Orleans, Louisiana, USA. Vector-Borne and Zoonotic Diseases 21 (10): 762–768. https://doi.org/10.1089/vbz.2021.0019.
[51]
Torres, C., and S. Hernández-Betancourt. 2016. Lesiones histológicas asociadas a la posible infección por Trypanosoma cruzi (Chagas, 1909) en corazones de roedores sinantrópicos capturados en Yucatán. Anales De Biología 38: 29–35. https://doi.org/10.6018/analesbio.38.03.
[52]
Tricco, Andrea C., Erin Lillie, Wasifa Zarin, Kelly K. O’Brien, Heather Colquhoun, Danielle Levac, David Moher, et al. 2018. The “PRISMA extension for scoping reviews (PRISMA-ScR): Checklist and explanation.” Annals of Internal Medicine. American College of Physicians. https://doi.org/10.7326/M18-0850.
[53]
Ucan-Euan, F., S. Hernández-Betancourt, M. Arjona-Torres, A. Panti-May, and M. Torres-Castro. 2019. Estudio histopatológico en tejido cardiaco de roedores infectados con Trypanosoma cruzi, capturados en barrios suburbanos, Mérida, México. Biomédica 39: 32–43. https://doi.org/10.7705/biomedica.v39i3.4192.
[54]
Villagrán, M.E., J.A. Martínez-Ibarra, and J.A. De Diego. 2011. Pathological alterations and prevalence of Trypanosoma cruzi in opossums from western Mexico. Boletin De Malariologia y Salud Ambiental 51 (1): 87–88. ISSN 1690-4648 Available in: http://ve.scielo.org/scielo.php?script=sci_arttext&pid=S169046482011000100010&lng=es&tlng=en
[55]
Vitelli-Avelar, D.M., R. Sathler-Avelar, A.M. Mattoso-Barbosa, N. Gouin, M. Perdig?o-de-Oliveira, L. Valerio-dos-Reis, R.P. Costa, S.M. Elói-Santos, M.D.S. Gomes, and L.R.D. Amaral. 2017. Cynomolgus macaques naturally infected with Trypanosoma cruzi-I exhibit an overall mixed proinflammatory/modulated cytokine signature characteristic of human Chagas disease. PLoS Neglected Tropical Diseases 11 (2): 1–18. https://doi.org/10.1371/journal.pntd.0005233.
[56]
Williams, J.T., E.J. Dick, J.L. VandeBerg, and G.B. Hubbard. 2009. Natural Chagas disease in four baboons. Journal of Medical Primatology 38 (2): 107–113. https://doi.org/10.1111/j.1600-0684.2008.00308.
[57]
Zecca, I.B., S.A. Hamer, S. Slack, L.D. Auckland, and C.L. Hodo. 2020. Trypanosoma cruzi infections and associated pathology in urban-dwelling Virginia opossums (Didelphis virginiana). International Journal for Parasitology: Parasites and Wildlife 11: 287–293. https://doi.org/10.1016/j.ijppaw.2020.03.004.
[58]
Zecca, I.B., C.L. Hodo, H.M. Swarts, T.W. DeMaar, K.F. Snowden, H.L. Prestridge, J.E. Light, and S.A. Hamer. 2021. Trypanosoma cruzi and incidental Sarcocystis spp. in endangered ocelots (Leopardus pardalis) of South Texas, USA. Journal of Wildlife Diseases 57 (3): 667–671. https://doi.org/10.7589/jwd-d-20-00169.
Funding
Consejo Nacional de Humanidades, Ciencias y Tecnología(106914)
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