Natural infection with Trypanosoma cruzi in bats captured in Campeche and Yucatán, México
Abstract
Introduction: Bats have been reported as hosts of the Trypanosoma cruzi protozoan, the etiologic agent of American trypanosomiasis, an endemic zoonotic disease in México.
Objective: To describe T. cruzi infection in bats from the states of Campeche and Yucatán, México.
Materials and methods: Captures were made from March to November, 2017, at three sites in Yucatán and one in Campeche. Up to four mist nets on two consecutive nights were used for the capture. The bats’ species were identified and euthanasia was performed to collect kidney and heart samples for total DNA extraction. Trypanosoma cruzi infection was detected by conventional PCR with the amplification of a fragment belonging to the T. cruzi DNA nuclear.
Results: Eighty-six bats belonging to five families (Vespertilionidae, Noctilionidae, Mormoopidae, Phyllostomidae, and Molossidae) and 13 species (Rhogeessa aeneus, Noctilio leporinus, Pteronotus davyi, P. parnellii, Artibeus jamaicensis, A. lituratus, A. phaeotis, Glossophaga soricina, Carollia sowelli, Chiroderma villosum, Uroderma bilobatum, Sturnira parvidens, and Molossus rufus) were captured. Infection frequency by PCR was 30,2% (26/86) detected only in the renal tissue. The infected species were P. parnellii, G. soricina, A. lituratus, A. jamaicensis, S. parvidens, C. villosum, and R. aeneus.
Conclusions: Our results confirmed the participation of several bat species as hosts in the T. cruzi transmission cycle in the region. Further studies are necessary to establish the importance of these animals in the zoonotic transmission of T. cruzi.
Downloads
References
Carrada-Bravo T. Trypanosoma cruzi: historia natural y diagnóstico de la enfermedad de Chagas. Rev Mex Patol Clin. 2004;51:205-19.
Salazar-Schettino PM, Cabrera-Bravo M, Vázquez-Antona C, Zenteno E, De Alba-Alvarado M, Torres-Gutiérrez E, et al. Chagas disease in Mexico: Report of 14 cases of chagasic cardiomyopathy in children. Tohoku J Exp Med. 2016;240:243-9. https://doi.org/10.1620/tjem.240.243
Waleckx E, Camara-Mejia J, Ramírez-Sierra MJ, Cruz-Chan V, Rosado-Vallado M, Vázquez-Narváez S, et al. An innovative ecohealth intervention for Chagas disease vector control in Yucatán, México. Trans R Soc Trop Med Hyg. 2015;109:143-9. https://doi.org/10.1093/trstmh/tru200
Dirección General de Epidemiología (DGE). Secretaría de Salud (SSA). Anuarios de morbilidad. Fecha de consulta: 12 de mayo del 2020. Disponible en: https://www.gob.mx/salud/documentos/datos-abiertos-152127?idiom=es
Nichols MD, Lord WD, Haynie ML, Brennan RE, Jackson VL, Monterroso WS. Trypanosoma cruzi in a Mexican free-tailed bat (Tadarida brasiliensis) in Oklahoma, USA. J Wildl Dis. 2019;55:444-8. https://doi.org/10.7589/2018-04-095
Bern C, Kjos S, Yabsley MJ, Montgomery SP. Trypanosoma cruzi and Chagas’ disease in the United States. Clin Microbiol Rev. 2011;24:655-81. https://doi.org/10.1128/CMR.00005-11
Mejía A, Portugal-García C, Chávez-López V, García-Vázquez Z, Ramos C. Evidencia serológica de infección por Trypanosoma cruzi en perros atendidos en clínicas veterinarias del área conurbada de Cuernavaca, Morelos. Salud Pública Mex. 2017;59:205-6. https://doi.org/10.21149/7945
Ruiz-Piña H, Gutiérrez-Ruiz E, Escobedo-Ortegón F, Rodríguez-Vivas R, Bolio-González M, Ucan-Leal D. Prevalence of Trypanosoma cruzi in backyard mammals from a rural comunity of Yucatán, México. Trop Subtrop Agroecosystems. 2018;21:367-71.
Panti-May JA, DE Andrade RRC, Gurubel-González Y, Palomo-Arjona E, Sodá-Tamayo L, Meza-Sulú J, et al. A survey of zoonotic pathogens carried by house mouse and black rat populations in Yucatán, México. Epidemiol Infect. 2017;145:2287-95. https://doi.org/10.1017/S0950268817001352
Ucan-Euan F, Hernández-Betancourt S, Arjona-Torres M, Panti-May A, Torres-Castro M. Estudio histopatológico de tejido cardiaco de roedores infectados con Trypanosoma cruzi capturados en barrios suburbanos de Mérida, México. Biomédica. 2019;39(Supl.2):32-43. https://doi.org/10.7705/biomedica.v39i3.4192
Sánchez O. Murciélagos de México. CONABIO. Biodiversitas. 1998;20:1-11.
Jones G, Jacobs DS, Kunz TH, Willig MR, Racey PA. Carpe noctem: The importance of bats as bioindicators. Endanger Species Res. 2009;8:93-115. https://doi.org/10.3354/esr00182
Hui-Ju H, Hong-Ling W, Chuan-Min Z, Fang-Fang C, Li-Mei L, Jian-Wei L, et al. Bats as reservoirs of severe emerging infectious diseases. Virus Res. 2015;205:1-6. https://doi.org/10.1016/j.virusres.2015.05.006
Torres-Castro M, Febles-Solís V, Hernández-Betancourt S, Noh-Pech H, Estrella E, Peláez-Sánchez R, et al. Leptospira patógenas en murciélagos de Campeche y Yucatán, México. Rev MVZ Cordoba. 2020;25:e1815. https://doi.org/10.21897/rmvz.1815
Torres-Castro M, Muñoz-Dueñas D, Hernández-Betancourt S, Bolio-González M, Noh-Pech H, Peláez-Sánchez R, et al. Infección con Toxoplasma gondii (Eucoccidiorida: Sarcocystidae) en murciélagos de Campeche y Yucatán, México. Rev Biol Trop. 2019;67:633-42. https://doi.org/10.15517/rbt.v67i2.35147
Pinto CM, Kalko EKV, Cottontail I, Wellinghausen N, Cottontail VM. TcBat a bat-exclusive lineage of Trypanosoma cruzi in the Panama Canal Zone, with comments on its classification and the use of the 18S rRNA gene for lineage identification. Infect Genet Evol. 2012;12:1328-32. https://doi.org/10.1016/j.meegid.2012.04.013
Pinto CM, Ocaña-Mayorga S, Tapia EE, Lobos SE, Zurita AP, Aguirre-Villacís F, et al. Bats, Trypanosomes, and Triatomines in Ecuador: New insights into the diversity, transmission, and origins of Trypanosoma cruzi and Chagas disease. PloS ONE. 2015;10:e0139999. https://doi.org/10.1371/journal.pone.0139999
Marinkelle CJ. Prevalence of Trypanosoma cruzi-like infection of Colombian bats. Ann Trop Med Parasitol. 1982;76:125-34. https://doi.org/10.1080/00034983.1982.11687517
Argibay HD, Orozco MM, Cardinal MV, Rinas MA, Arnaiz M, Mena-Segura C, et al. First finding of Trypanosoma cruzi II in vampire bats from a district free of domestic vector-borne transmission in northeastern Argentina. Parasitology. 2016;143:1358-68. https://doi.org/10.1017/S0031182016000925
López-Cancino SA, Tun-Ku E, De la Cruz-Felix HK, Ibarra-Cerdeña CN, Izeta-Alberdi A, Pech-May A, et al. Landscape ecology of Trypanosoma cruzi in the southern Yucatan Peninsula. Acta Trop. 2015;151:58-72. https://doi.org/10.1016/j.actatropica.2015.07.021
Hodo CL, Goodwin CC, Mayes BC, Mariscal JA, Waldrup KA, Hamer SA. Trypanosome species, including Trypanosoma cruzi, in sylvatic and peridomestic bats of Texas, USA. Acta Trop. 2016;164:259-66. https://doi.org/10.1016/j.actatropica.2016.09.013
Secretaría de Fomento Económico (SEFOE). Tzucacab. Fecha de consulta: 10 de agosto del 2019. Disponible en: http://www.sefoe.yucatan.gob.mx/secciones/ver/tzucacab
Martínez-Noble JI, Meléndez-Ramírez V, Delfín-González H, Pozo C. Mariposas de la selva mediana subcaducifolia de Tzucacab, con nuevos registros para Yucatán, México. Rev Mex Biodivers. 2015;86:348-57. https://doi.org/10.1016/j.rmb.2015.04.010
Gutiérrez-Báez C, Zamora-Crescencio P, Puc-Garrido E. Estructura y composición florística de la selva mediana subperennifolia de Hampolol, Campeche, México. For Ver. 2013;15:1-8.
Secretaría de Fomento Económico (SEFOE). Panabá. Fecha de consulta: 10 de agosto del 2019. Disponible en: http://www.sefoe.yucatan.gob.mx/secciones/ver/panaba
Magaña-Rueda S, Santos-Flores J, Castillo-Caamal J. Identificación y uso de la vegetación nativa en ranchos de doble propósito en el Oriente de Yucatán. Bioagrociencias. 2015;8:17-22.
Simei M, Campos B, Jiménez-Osornio J, Barrientos MR. Fenología y producción de frutos de plantaciones de siricote (Cordia dodecandra A. DC.) bajo tres tipos de manejo en X’matkuil, Yucatán, México. Polibotánica. 2016;41:115-31. https://doi.org/10.18387/polibotanica.41.8
Panti-May JA, Hernández-Betancourt S, Ruiz-Piña H, Medina-Peralta S. Abundance and population parameters of commensal rodents present in rural households in Yucatan, Mexico. Int Biodeter Biodegr. 2012;66:77-81. https://doi.org/10.1016/j.ibiod.2011.10.006
Leary S, Underwood W, Cartner S, Corey D, Grandin T, Greenacre C, et al. AVMA Guidelines for the euthanasia of animals: 2013 edition. Illinois (USA): American Veterinary Medical Association; 2013. p. 102.
Medellín RA, Arita WHT, Sánchez O. Identificación de los murciélagos de México: clave de campo. México: Asociación Mexicana de Mastozoología, A.C.; 1997. p. 83.
Reid F. A field guide to the mammals of America Central and Southeast México. Second edition. New York: Oxford University Press; 2009. p. 384.
Moser DR, Kirchhoff LV, Donelson JE. Detection of Trypanosoma cruzi by DNA amplification using the polymerase chain reaction. J Clin Microbiol. 1989;27:1477-82.
Sosa-Escalante JE, Hernández-Betancourt S, Pech-Canché JM, MacSwiney GCM, Díaz-Gamboa R. Los mamíferos del estado de Yucatán. Rev Mexicana Mastozoo (Nueva Época). 2014;4:40-59. https://doi.org/10.22201/ie.20074484e.2014.4.1.190
Ortega J, Castro-Arellano I. Artibeus jamaicensis. Mamm species. 2001;662:1-9.
Córdova-Aldana D, Escobedo-Ortegón JE, Hernández-Betancourt S, Ruiz-Piña HA. Los murciélagos en el ciclo de transmisión de Trypanosoma cruzi en el peridomicilio rural. En: Pacheco-Castro J, Lugo-Pérez JA, Tzuc-Canché L, Ruíz-Piña HA editores. Estudios multidisciplinarios de las enfermedades zoonóticas y ETVs en Yucatán. Mérida (México): Ediciones de la Universidad Autónoma de Yucatán; 2013. p. 233-46.
Villegas-García JC, Santillán-Alarcón S. Sylvatic focus of American Trypanosomiasis in the State of Morelos, México. Rev Biol Trop. 2001;49:685-8.
Villena FE, Gómez-Puerta LA, Jhonston EJ, Del Alcázar OM, Maguiña JL, Albujar C, et al. First report of Trypanosoma cruzi infection in salivary gland of bats from the Peruvian Amazon. Am J Trop Med Hyg. 2018;99:723-8. https://doi.org/10.4269/ajtmh.17-0816
Ramírez JD, Hernández C, Montilla M, Zambrano P, Flórez AC, Parra E, et al. First report of human Trypanosoma cruzi infection attributed to TcBat genotype. Zoonoses Public Health. 2014;61:477-9. https://doi.org/10.1111/zph.12094
Dos Santos FCB, Lisboa CV, Xavier SCC, Dario MA, Verde RS, Calouro AM, et al. Trypanosoma sp. diversity in Amazonian bats (Chiroptera; Mammalia) from Acre State, Brazil. Parasitology. 2018;145:828-37. https://doi.org/10.1017/S0031182017001834
Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas’ disease. Bull Am Mus Nat Hist. 1979;163:123-520.
Oliveira MA, Lopes-Ferreira R, Carneiro MA, Diotaiuti L. Ecology of Cavernicola pilosa Barber, 1937 (Hemiptera: Reduviidae: Triatominae) in the Boa Esperança cave, Tocantins, Brazil. Ecotropica. 2008;14:63-8.
Reyes-Novelo E, Ruiz-Piña H, Escobedo-Ortegón J, Barrera-Pérez M, Manrique-Saide P, Rodríguez-Vivas RI. Triatoma dimidiata (Latreille) abundance and infection with Trypanosoma cruzi in a rural community of Yucatan, Mexico. Neotrop Entomol. 2013;42:317-24. https://doi.org/10.1007/s13744-013-0120-x
Dumonteil E, Gourbière S, Barrera-Pérez M, Rodríguez-Félix E, Ruiz-Piña H, Baños-López O, et al. Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruzi in the Yucatán, peninsula of México. Am J Trop Med Hyg. 2002;67:176-83. https://doi.org/10.4269/ajtmh.2002.67.176
Dumonteil E, Ramírez-Sierra MJ, Pérez-Carrillo S, Teh-Poot C, Herrera C, Gourbière S, et al. Detailed ecological associations of triatomines revealed by metabarcoding and next-generation sequencing: Implications for triatomine behavior and Trypanosoma cruzi transmission cycles. Sci Rep. 2018;8:4140. https://doi.org/10.1038/s41598-018-22455-x
Thomas ME, Rasweiler IV JJ, D’Alessandro A. Experimental transmission of the parasitic flagellates Trypanosoma cruzi and Trypanosoma rangeli between triatomine bugs or mice and captive neotropical bats. Mem Inst Oswaldo Cruz. 2007;102:559-65. https://doi.org/10.1590/s0074-02762007005000068
Añez N, Crisante G, Soriano PJ. Trypanosoma cruzi congenital transmission in wild bats. Acta Trop. 2009;109:78-80. https://doi.org/10.1016/j.actatropica.2008.08.009
Martínez-Díaz RA, Escario JA, Nogal-Ruiz JJ, Gómez-Barrio A. Biological characterization of Trypanosoma cruzi strains. Mem Inst Oswaldo Cruz. 2001;96:53-9. https://doi.org/10.1590/s0074-02762001000100006
Roellig DM, Yabsley MJ. Infectivity, pathogenicity, and virulence of Trypanosoma cruzi isolates from sylvatic animals and vectors, and domestic dogs from the United States in ICR strain mice and SD strain rats. Am J Trop Med Hyg. 2010; 83:519-22. https://doi.org/10.4269/ajtmh.2010.09-0663
Andrade LO, Machado CRS, Chiari E, Pena SDJ, Macedo AM. Differential tissue distribution of diverse clones of Trypanosoma cruzi in infected mice. Mol Biochem Parasitol. 1999;100:163-72. https://doi.org/10.1016/s0166-6851(99)90035-x
Zúñiga C, Vargas R, Vergara U. Evolución de la infección con Trypanosoma cruzi en cepas susceptibles y resistentes de ratones. Arch Med Vet. 2002;34:183-8. http://dx.doi.org/10.4067/S0301-732X2002000200004
Some similar items:
- Paula Ximena Pavía, Nubia Lucía Roa, Ana María Uribe, Concepción Judith Puerta, Using S35-S36 and TcH2AF-R primer-based PCR tests to follow-up a Chagas’ disease patient who had undergone a heart transplant , Biomedica: Vol. 31 No. 2 (2011)
- Ernesto Pérez-Sánchez, Raúl Montiel-Cruz, Eréndira Romero-Domínguez, Griselda Pascacio-Bermúdez, Arturo Báez-Hernández, Guadalupe Díaz del Castillo-Flores, Fabián Correa-Morales, Gonzalo Vázquez-Prokopec, Pablo Manrique-Saide, Azael Che-Mendoza, Gabriela Meneses-Ruiz , Irma López-Martínez, María Jesús Sánchez, Seroprevalence of Trypanosoma cruzi among children from Veracruz, Mexico: Epidemiological baseline for a control model based on Chagas disease active transmission , Biomedica: Vol. 44 No. 1 (2024)
- Lizbeth Díaz, Karen Covarrubias, Ángel Licón, Mixtli Astorga, Yaneth Moreno, José Alejandro Martínez, Biological parameters of Meccus phyllosomus phyllosomus (Burmeister), 1835, Triatoma recurva (Stål), 1868 (Hemiptera, Reduviidae) and their laboratory hybrids , Biomedica: Vol. 37 No. Sup. 2 (2017): Suplemento 2, Entomología médica, 2017
- Juliana Gil, Paula Pavía, Marleny Montilla, Astrid C. Florez, Claudia Quintero, Marcela Mercado, Miguel Vacca, Santiago Nicholls, Concepción Puerta, Comparison of a PCR test based on the histone H2A/SIRE genes with classical serological tests for the diagnosis of chronic Chagas disease in Colombian patients , Biomedica: Vol. 27 No. 1esp (2007): Enfermedad de Chagas
- Liliana Torcoroma García, Jhancy Rocío Aguilar, Marly Yojhana Bueno , Erika Marcela Moreno, Herminia Ramírez , Nelson Daza , Disagreement between PCR and serological diagnosis of Trypanosoma cruzi infection in blood donors from a Colombian endemic region , Biomedica: Vol. 41 No. Supl. 1 (2021): Mayo, Parasitología médica
- Mayra L. Lúa, Arturo Plascencia, Patricia Paredes, Yaxsier de Armas, Miguel Raygoza, Erika Martínez, Fernando Siller, Iván Isidro Hernández, Etiological identification of viral agents in acute encephalitis in Guadalajara, México, 2011-2015 , Biomedica: Vol. 38 No. 2 (2018)
- Concepción Judith Puerta, Johana María Guevara, Paula Ximena Pavía, Marleny Montilla, Rubén Santiago Nicholls, Edgar Parra, Yuli Katherine Barrera, Evaluation of TcH2AF-R and S35-S36 primers in PCR tests for the detection of Trypanosoma cruzi in mouse cardiac tissue , Biomedica: Vol. 28 No. 4 (2008)
- Mónica Llano, Paula Pavía, Astrid Carolina Flórez, Adriana Cuéllar, John Mario González, Concepción Judith Puerta, Preliminary evaluation of the commercial kit Chagas (Trypanosoma cruzi) IgG-ELISA® in Colombian individuals , Biomedica: Vol. 34 No. 2 (2014)
- Rubén Santiago Nicholls, Zulma Milena Cucunubá, Angélica Knudson, Astrid Carolina Flórez, Marleny Montilla, Concepción Judith Puerta, Paula Ximena Pavía, Acute Chagas disease in Colombia: a rarely suspected disease. Report of 10 cases presented during the 2002-2005 period , Biomedica: Vol. 27 No. 1esp (2007): Enfermedad de Chagas
- Concepción Judith Puerta, Paula Ximena Pavia, Marleny Montilla, Carolina Flórez, Giomar Herrera, Juan Manuel Ospina, Fred Manrique, Rubén Santiago Nicholls, The first case of congenital Chagas’ disease analyzed by AP-PCR in Colombia , Biomedica: Vol. 29 No. 4 (2009)
Article metrics | |
---|---|
Abstract views | |
Galley vies | |
PDF Views | |
HTML views | |
Other views |