Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia

Chagas disease remains a major neglected disease in Colombia. We aimed to characterize Trypanosoma cruzi transmission networks in the Sierra Nevada de Santa Marta (SNSM) region, to shed light on disease ecology and help optimize control strategies. Triatomines were collected in rural communities and...

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Autores:
Murillo Solano, Claribel
López Domínguez, Jaime
Gongora, Rafael
Rojas Gulloso, Andrés Camilo
Usme Ciro, José Aldemar
Perdomo Balaguera, Erick
Herrera, Claudia
Parra Henao, Gabriel
Dumonteil, Eric
Tipo de recurso:
Article of investigation
Fecha de publicación:
2021
Institución:
Universidad Cooperativa de Colombia
Repositorio:
Repositorio UCC
Idioma:
OAI Identifier:
oai:repository.ucc.edu.co:20.500.12494/46838
Acceso en línea:
https://doi.org/10.1038/s41598-021-91783-2
https://hdl.handle.net/20.500.12494/46838
Palabra clave:
Trypanosoma cruzi
Sierra Nevada de Santa Marta
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openAccess
License
Atribución
id COOPER2_675e57581297166a3c096290f609c27d
oai_identifier_str oai:repository.ucc.edu.co:20.500.12494/46838
network_acronym_str COOPER2
network_name_str Repositorio UCC
repository_id_str
dc.title.spa.fl_str_mv Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia
title Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia
spellingShingle Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia
Trypanosoma cruzi
Sierra Nevada de Santa Marta
title_short Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia
title_full Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia
title_fullStr Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia
title_full_unstemmed Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia
title_sort Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia
dc.creator.fl_str_mv Murillo Solano, Claribel
López Domínguez, Jaime
Gongora, Rafael
Rojas Gulloso, Andrés Camilo
Usme Ciro, José Aldemar
Perdomo Balaguera, Erick
Herrera, Claudia
Parra Henao, Gabriel
Dumonteil, Eric
dc.contributor.author.none.fl_str_mv Murillo Solano, Claribel
López Domínguez, Jaime
Gongora, Rafael
Rojas Gulloso, Andrés Camilo
Usme Ciro, José Aldemar
Perdomo Balaguera, Erick
Herrera, Claudia
Parra Henao, Gabriel
Dumonteil, Eric
dc.subject.spa.fl_str_mv Trypanosoma cruzi
Sierra Nevada de Santa Marta
topic Trypanosoma cruzi
Sierra Nevada de Santa Marta
description Chagas disease remains a major neglected disease in Colombia. We aimed to characterize Trypanosoma cruzi transmission networks in the Sierra Nevada de Santa Marta (SNSM) region, to shed light on disease ecology and help optimize control strategies. Triatomines were collected in rural communities and analyzed for blood feeding sources, parasite diversity and gut microbiota composition through a metagenomic and deep sequencing approach. Triatoma dimidiata predominated, followed by Rhodnius prolixus, Triatoma maculata, Rhodnius pallescens, Panstrongylus geniculatus and Eratyrus cuspidatus. Twenty-two species were identified as blood sources, resulting in an integrated transmission network with extensive connectivity among sylvatic and domestic host species. Only TcI parasites were detected, predominantly from TcIb but TcIa was also reported. The close relatedness of T. cruzi strains further supported the lack of separate transmission cycles according to habitats or triatomine species. Triatomine microbiota varied according to species, developmental stage and T. cruzi infection. Bacterial families correlated with the presence/absence of T. cruzi were identified. In conclusion, we identified a domestic transmission cycle encompassing multiple vector species and tightly connected with sylvatic hosts in the SNSM region, rather than an isolated domestic transmission cycle. Therefore, integrated interventions targeting all vector species and their contact with humans should be considered.
publishDate 2021
dc.date.issued.none.fl_str_mv 2021-06-10
dc.date.accessioned.none.fl_str_mv 2022-10-22T16:25:50Z
dc.date.available.none.fl_str_mv 2022-10-22T16:25:50Z
dc.type.none.fl_str_mv Artículos Científicos
dc.type.coar.none.fl_str_mv http://purl.org/coar/resource_type/c_2df8fbb1
dc.type.coarversion.none.fl_str_mv http://purl.org/coar/version/c_970fb48d4fbd8a85
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dc.identifier.issn.spa.fl_str_mv 2045-2322
dc.identifier.uri.spa.fl_str_mv https://doi.org/10.1038/s41598-021-91783-2
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12494/46838
dc.identifier.bibliographicCitation.spa.fl_str_mv Murillo-Solano, C., López-Domínguez, J., Gongora, R. et al.(2021) Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia. Sci Rep 11, 12306 (2021). https://doi.org/10.1038/s41598-021-91783-2.https://repository.ucc.edu.co/handle/20.500.12494/46838
identifier_str_mv 2045-2322
Murillo-Solano, C., López-Domínguez, J., Gongora, R. et al.(2021) Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia. Sci Rep 11, 12306 (2021). https://doi.org/10.1038/s41598-021-91783-2.https://repository.ucc.edu.co/handle/20.500.12494/46838
url https://doi.org/10.1038/s41598-021-91783-2
https://hdl.handle.net/20.500.12494/46838
dc.relation.isversionof.spa.fl_str_mv https://www.nature.com/articles/s41598-021-91783-2#Bib1
dc.relation.ispartofjournal.spa.fl_str_mv Scientific Reports
dc.relation.references.spa.fl_str_mv Hotez, P. J. et al. An unfolding tragedy of chagas disease in North America. PLoS Negl. Trop. Dis. 7(10), e2300. https://doi.org/10.1371/journal.pntd.0002300 (2013) (PMID: 24205411).
Hotez, P. J., Bottazzi, M. E., Franco-Paredes, C., Ault, S. K. & Periago, M. R. The neglected tropical diseases of Latin America and the Caribbean: A review of disease burden and distribution and a roadmap for control and elimination. PLoS Negl. Trop. Dis. 2(9), e300. https://doi.org/10.1371/journal.pntd.0000300 (2008) (PMID: 18820747).
Lee, B. Y., Bacon, K. M., Bottazzi, M. E. & Hotez, P. J. Global economic burden of Chagas disease: A computational simulation model. Lancet Infect. Dis. 13(4), 342–348. https://doi.org/10.1016/S1473-3099(13)70002-1 (2013) (PMID: 23395248).
WHO. Chagas disease in Latin America: An epidemiological update based on 2010 estimates. Wkly. Epidemiol. Rec. 90(6), 33–43 (2015) (PMID: 25671846).
Pena-Garcia, V. H., Gomez-Palacio, A. M., Triana-Chavez, O. & Mejia-Jaramillo, A. M. Eco-epidemiology of Chagas disease in an endemic area of Colombia: Risk factor estimation, Trypanosoma cruzi characterization and identification of blood-meal sources in bugs. Am. J. Trop. Med. Hyg. 91(6), 1116–1124. https://doi.org/10.4269/ajtmh.14-0112 (2014) (PMID: 25331808).
Mejia-Jaramillo, A. M. et al. Genotyping of Trypanosoma cruzi in a hyper-endemic area of Colombia reveals an overlap among domestic and sylvatic cycles of Chagas disease. Parasit. Vectors. 7, 108. https://doi.org/10.1186/1756-3305-7-108 (2014) (PMID: 24656115).
Dib, J. C., Agudelo, L. A. & Velez, I. D. Prevalencia de patologías tropicales y factores de riesgo en la comunidad indígena de Bunkwimake, Sierra Nevada de Santa Marta. DUAZARY. 3(1), 38–44 (2006).
Parra-Henao, G. et al. In search of congenital Chagas disease in the Sierra Nevada de Santa Marta, Colombia. Am. J. Trop. Med. Hyg. 101(3), 482–483. https://doi.org/10.4269/ajtmh.19-0110 (2019) (PMID: 31264558).
Guhl, F., Aguilera, G., Pinto, N. & Vergara, D. Actualización de la distribución geográfica y ecoepidemiología de la fauna de triatominos (Reduviidae: Triatominae) en Colombia. Biomedica. 27(Suppl 1), 143–162 (2007) (PMID: 18154255).
Parra-Henao, G., Suarez-Escudero, L. C. & Gonzalez-Caro, S. Potential distribution of Chagas disease vectors (Hemiptera, Reduviidae, Triatominae) in Colombia, based on Ecological Niche Modeling. J. Trop. Med. 2016, 1439090. https://doi.org/10.1155/2016/1439090 (2016) (PMID: 28115946).
Rodriguez-Mongui, E., Cantillo-Barraza, O., Prieto-Alvarado, F. E. & Cucunuba, Z. M. Heterogeneity of Trypanosoma cruzi infection rates in vectors and animal reservoirs in Colombia: A systematic review and meta-analysis. Parasit. Vectors. 12(1), 308. https://doi.org/10.1186/s13071-019-3541-5 (2019) (PMID: 31221188).
Dib, J., Barnabe, C., Tibayrenc, M. & Triana, O. Incrimination of Eratyrus cuspidatus (Stal) in the transmission of Chagas’ disease by molecular epidemiology analysis of Trypanosoma cruzi isolates from a geographically restricted area in the north of Colombia. Acta Trop. 111(3), 237–242. https://doi.org/10.1016/j.actatropica.2009.05.004 (2009) (PMID: 19442641).
Parra Henao, G., Angulo, V., Jaramillo, N. & Restrepo, M. Triatominos (Hemiptera: Reduviidae) de ka Sierra Nevada de Santa Marta, Colombia. Aspectos epidemiológicos, entomológicos y de distribución. Rev. CES Med. 23(1), 17–26 (2009).
Hernandez, C. et al. Untangling the transmission dynamics of primary and secondary vectors of Trypanosoma cruzi in Colombia: Parasite infection, feeding sources and discrete typing units. Parasit. Vectors. 9(1), 620. https://doi.org/10.1186/s13071-016-1907-5 (2016) (PMID: 27903288).
Cantillo-Barraza, O., Chaverra, D., Marcet, P., Arboleda-Sanchez, S. & Triana-Chavez, O. Trypanosoma cruzi transmission in a Colombian Caribbean region suggests that secondary vectors play an important epidemiological role. Parasit. Vectors. 7, 381. https://doi.org/10.1186/1756-3305-7-381 (2014) (PMID: 25141852).
Weiss, B. & Aksoy, S. Microbiome influences on insect host vector competence. Trends Parasitol. 27(11), 514–522. https://doi.org/10.1016/j.pt.2011.05.001 (2011) (PMID: 21697014).
Azambuja, P., Garcia, E. S. & Ratcliffe, N. A. Gut microbiota and parasite transmission by insect vectors. Trends Parasitol. 21(12), 568–572 (2005) (PMID: 16226491).
Dumonteil, E. et al. Interactions among Triatoma sanguisuga blood feeding sources, gut microbiota and Trypanosoma cruzi diversity in southern Louisiana. Mol Ecol. 29(19), 3747–3761 (2020).
Zingales, B. et al. A new consensus for Trypanosoma cruzi intraspecific nomenclature: Second revision meeting recommends TcI to TcVI. Mem. Inst. Oswaldo Cruz. 104(7), 1051–1054 (2009) (PMID: 20027478).
Zingales, B. et al. The revised Trypanosoma cruzi subspecific nomenclature: Rationale, epidemiological relevance and research applications. Infect. Genet. Evol. 12(2), 240–253. https://doi.org/10.1016/j.meegid.2011.12.009 (2012) (PMID: 22226704).
Tibayrenc, M. & Ayala, F. J. The population genetics of Trypanosoma cruzi revisited in the light of the predominant clonal evolution model. Acta Trop. 151, 156–165. https://doi.org/10.1016/j.actatropica.2015.05.006 (2015) (PMID: 26188332).
Majeau, A., Murphy, L., Herrera, C. & Dumonteil, E. Assessing Trypanosoma cruzi parasite diversity through comparative genomics: Implications for disease epidemiology and diagnostics. Pathogens. 10, 212. https://doi.org/10.3390/pathogens10020212 (2021).
Flores-Ferrer, A., Marcou, O., Waleckx, E., Dumonteil, E. & Gourbière, S. Evolutionary ecology of Chagas disease; what do we know and what do we need?. Evol. Appl. 11(4), 470–487. https://doi.org/10.1111/eva.12582 (2017).
Tibayrenc, M., Kjellberg, F. & Ayala, F. J. A clonal theory of parasitic protozoa: The population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas, and Trypanosoma and their medical and taxonomical consequences. Proc. Natl. Acad. Sci. USA 87, 2414–2418 (1990).
Berry, A. S. F. et al. Sexual reproduction in a natural Trypanosoma cruzi population. PLoS Negl. Trop. Dis. 13(5), e0007392. https://doi.org/10.1371/journal.pntd.0007392 (2019) (PMID: 31107905).
Schwabl, P. et al. Meiotic sex in Chagas disease parasite Trypanosoma cruzi. Nat. Commun. 10(1), 3972. https://doi.org/10.1038/s41467-019-11771-z (2019) (PMID: 31481692).
Falla, A. et al. Haplotype identification within Trypanosoma cruzi I in Colombian isolates from several reservoirs, vectors and humans. Acta Trop. 110(1), 15–21 (2009) (PMID: 19135020).
Cura, C. I. et al. Trypanosoma cruzi I genotypes in different geographical regions and transmission cycles based on a microsatellite motif of the intergenic spacer of spliced-leader genes. Int. J. Parasitol. 40(14), 1599–1607. https://doi.org/10.1016/j.ijpara.2010.06.006 (2010) (PMID: 20670628).
Rodriguez, I. B. et al. Transmission dynamics of Trypanosoma cruzi determined by low-stringency single primer polymerase chain reaction and southern blot analyses in four indigenous communities of the Sierra Nevada de Santa Marta, Colombia. Am. J. Trop. Med. Hyg. 81(3), 396–403 (2009) (PMID: 19706903).
Waleckx, E., Gourbière, S. & Dumonteil, E. Intrusive triatomines and the challenge of adapting vector control practices. Mem. Inst. Oswaldo Cruz. 110(3), 324–338 (2015).
Dumonteil, E. 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. 8(1), 4140. https://doi.org/10.1038/s41598-018-22455-x (2018) (PMID: 29515202).
Dumonteil, E. et al. Interactions among Triatoma sanguisuga blood feeding sources, gut microbiota and Trypanosoma cruzi diversity in southern Louisiana. Mol. Ecol. https://doi.org/10.1111/mec.15582 (2020) (PMID: 32749727).
O’Connor, O., Bosseno, M. F., Barnabe, C., Douzery, E. J. & Breniere, S. F. Genetic clustering of Trypanosoma cruzi I lineage evidenced by intergenic miniexon gene sequencing. Infect. Genet. Evol. 7(5), 587–593. https://doi.org/10.1016/j.meegid.2007.05.003 (2007) (PMID: 17553755).
Villanueva-Lizama, L., Teh-Poot, C., Majeau, A., Herrera, C. & Dumonteil, E. Molecular genotyping of Trypanosoma cruzi by next-generation sequencing of the mini-exon gene reveals infections with multiple parasite DTUs in Chagasic patients from Yucatan, Mexico. J. Inf. Dis. 219(12), 1980–1988 (2019).
Parra-Henao, G., Angulo, V. M., Osorio, L. & Jaramillo, O. N. Geographic distribution and ecology of Triatoma dimidiata (Hemiptera: Reduviidae) in Colombia. J. Med. Entomol. 53(1), 122–129. https://doi.org/10.1093/jme/tjv163 (2016) (PMID: 26487247).
Angulo, V. M., Esteban, L. & Luna, K. P. Attalea butyracea proximas a las viviendas como posible fuente de infestacion domiciliaria por Rhodnius prolixus (Hemiptera: Reduviidae) en los Llanos Orientales de Colombia. Biomedica. 32(2), 277–285. https://doi.org/10.1590/S0120-41572012000300016 (2012) (PMID: 23242302).
Feliciangeli, M. D., Sanchez-Martin, M., Marrero, R., Davies, C. & Dujardin, J. P. Morphometric evidence for a possible role of Rhodnius prolixus from palm trees in house re-infestation in the State of Barinas (Venezuela). Acta Trop. 101(2), 169–177. https://doi.org/10.1016/j.actatropica.2006.12.010 (2007) (PMID: 17306204).
Fitzpatrick, S., Feliciangeli, M. D., Sanchez-Martin, M. J., Monteiro, F. A. & Miles, M. A. Molecular genetics reveal that silvatic Rhodnius prolixus do colonise rural houses. PLoS Negl. Trop. Dis. 2(4), e210. https://doi.org/10.1371/journal.pntd.0000210 (2008) (PMID: 18382605).
Lopez, G. & Moreno, J. Genetic variability and differentiation between populations of Rhodnius prolixus and R. pallescens, vectors of Chagas’ disease in Colombia. Mem. Inst. Oswaldo Cruz. 90, 353–357 (1995).
Dumonteil, E. et al. Detailed ecological associations of triatomines revealed by metabarcoding based on next-generation sequencing: linking triatomine behavioral ecology and Trypanosoma cruzi transmission cycles. Sci. Rep. 8(1), 4140. https://doi.org/10.1038/s41598-018-22455-x (2018).
Hernández-Andrade, A., Moo-Millan, J., Cigarroa-Toledo, N., Ramos-Ligonio, A., Herrera, C., Bucheton, B., et al. Metabarcoding: A powerful yet still underestimated approach for the comprehensive study of vector-borne pathogen transmission cycles and their dynamics. in Vector-Borne Diseases: Recent Developments in Epidemiology and Control (ed. Claborn, D.) 1–6. (Intechopen, 2020). https://doi.org/10.5772/intechopen.83110
Flores-Ferrer, A., Waleckx, E., Rascalou, G., Dumonteil, E. & Gourbière, S. Trypanosoma cruzi transmission dynamics in a synanthropic and domesticated host community. PLoS Negl. Trop. Dis. 13(12), e0007902. https://doi.org/10.1371/journal.pntd.0007902 (2019).
Llewellyn, M. S. et al. Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathog. 5(5), e1000410. https://doi.org/10.1371/journal.ppat.1000410 (2009) (PMID: 19412340).
Herrera, C. et al. Genetic variability and phylogenetic relationships within Trypanosoma cruzi I isolated in Colombia based on Miniexon Gene Sequences. J. Parasitol. Res. https://doi.org/10.1155/2009/897364 (2009) (PMID: 20798881).
Zumaya-Estrada, F. A. et al. North American import? Charting the origins of an enigmatic Trypanosoma cruzi domestic genotype. Parasit. Vectors. 5, 226. https://doi.org/10.1186/1756-3305-5-226 (2012) (PMID: 23050833).
Montoya-Porras, L. M., Omar, T. C., Alzate, J. F., Moreno-Herrera, C. X. & Cadavid-Restrepo, G. E. 16S rRNA gene amplicon sequencing reveals dominance of Actinobacteria in Rhodnius pallescens compared to Triatoma maculata midgut microbiota in natural populations of vector insects from Colombia. Acta Trop. 178, 327–332. https://doi.org/10.1016/j.actatropica.2017.11.004 (2018) (PMID: 29154947).
Kieran, T. J. et al. Regional biogeography of microbiota composition in the Chagas disease vector Rhodnius pallescens. Parasit. Vectors. 12(1), 504. https://doi.org/10.1186/s13071-019-3761-8 (2019) (PMID: 31665056).
Rodriguez-Ruano, S. M. et al. Microbiomes of North American Triatominae: The grounds for Chagas Disease epidemiology. Front. Microbiol. 9, 1167. https://doi.org/10.3389/fmicb.2018.01167 (2018) (PMID: 29951039).
Eichler, S. & Schaub, G. A. Development of symbionts in triatomine bugs and the effects of infections with trypanosomatids. Exp. Parasitol. 100(1), 17–27 (2002).
Waltmann, A. et al. Hindgut microbiota in laboratory-reared and wild Triatoma infestans. PLoS Negl. Trop. Dis. 13(5), e0007383. https://doi.org/10.1371/journal.pntd.0007383 (2019) (PMID: 31059501).
Herren, J. K. et al. A microsporidian impairs Plasmodium falciparum transmission in Anopheles arabiensis mosquitoes. Nat. Commun. 11(1), 2187. https://doi.org/10.1038/s41467-020-16121-y (2020) (PMID: 32366903).
Moreira, L. A. et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139(7), 1268–1278. https://doi.org/10.1016/j.cell.2009.11.042 (2009) (PMID: 20064373).
Angulo, V. M. & Esteban, L. Nueva trampa para la captura de triatominos en habitats silvestres y peridomesticos. Biomedica. 31(2), 264–268. https://doi.org/10.1590/S0120-41572011000200015 (2011) (PMID: 22159544).
Lent, H. & Wygodzinsky, P. Revision of Triatominae (Hemiptera: Reduviidae), and their significance as vectors of Chagas’ disease. Bull. Am. Mus. Nat. His. 163, 123–520 (1979).
Monteiro, F. A. et al. Molecular phylogeography of the Amazonian Chagas disease vectors Rhodnius prolixus and R. robustus. Mol. Ecol. 12(4), 997–1006. https://doi.org/10.1046/j.1365-294x.2003.01802.x (2003) (PMID: 12753218).
Baker, G. C., Smith, J. J. & Cowan, D. A. Review and reanalysis of domain-specific 16s primers. J. Microbiol. Meth. 55, 541–555 (2003).
Heuer, H., Krsek, M., Baker, P., Smalla, K. & Wellington, E. M. Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl. Environ. Microbiol. 63(8), 3233–3241 (1997).
Souto, R. P., Fernandes, O., Macedo, A. M., Campbell, D. A. & Zingales, B. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol. Biochem. Parasitol. 83(2), 141–152 (1996) (PMID: 9027747).
Majeau, A., Herrera, C. & Dumonteil, E. An improved approach to Trypanosoma cruzi molecular genotyping by next-generation sequencing of the mini-exon gene. Methods Mol. Biol. 1955, 47–60 (2019).
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16), 2194–2200. https://doi.org/10.1093/bioinformatics/btr381 (2011) (PMID: 21700674).
Garrison E, Marth G. Haplotype-based variant detection from short-read sequencing. arXiv preprint. (arXiv:1207.3907 [q-bio.GN]), 1–9. https://arxiv.org/abs/1207.3907v2 (2012).
Dhariwal, A. et al. MicrobiomeAnalyst: A web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res. 45(W1), W180–W188. https://doi.org/10.1093/nar/gkx295 (2017) (PMID: 28449106).
Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—Approximately maximum-likelihood trees for large alignments. PLoS ONE 5(3), e9490. https://doi.org/10.1371/journal.pone.0009490 (2010) (PMID: 20224823).
Bouckaert, R. et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol. 15(4), e1006650. https://doi.org/10.1371/journal.pcbi.1006650 (2019) (PMID: 30958812).
Torres-Silva, C. F. et al. Assessment of genetic mutation frequency induced by oxidative stress in Trypanosoma cruzi. Genet Mol Biol. 41(2), 466–474. https://doi.org/10.1590/1678-4685-GMB-2017-0281 (2018) (PMID: 30088612).
Hammer, Ø., Harper, D. A. T. & Ryan, P. D. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4(1), 9 (2001).
Cole, J. R. et al. Ribosomal Database Project: Data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42(Database issue), D633–D642. https://doi.org/10.1093/nar/gkt1244 (2014) (PMID: 24288368).
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spelling Murillo Solano, ClaribelLópez Domínguez, JaimeGongora, RafaelRojas Gulloso, Andrés CamiloUsme Ciro, José AldemarPerdomo Balaguera, ErickHerrera, ClaudiaParra Henao, GabrielDumonteil, Eric112022-10-22T16:25:50Z2022-10-22T16:25:50Z2021-06-102045-2322https://doi.org/10.1038/s41598-021-91783-2https://hdl.handle.net/20.500.12494/46838Murillo-Solano, C., López-Domínguez, J., Gongora, R. et al.(2021) Diversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in Colombia. Sci Rep 11, 12306 (2021). https://doi.org/10.1038/s41598-021-91783-2.https://repository.ucc.edu.co/handle/20.500.12494/46838Chagas disease remains a major neglected disease in Colombia. We aimed to characterize Trypanosoma cruzi transmission networks in the Sierra Nevada de Santa Marta (SNSM) region, to shed light on disease ecology and help optimize control strategies. Triatomines were collected in rural communities and analyzed for blood feeding sources, parasite diversity and gut microbiota composition through a metagenomic and deep sequencing approach. Triatoma dimidiata predominated, followed by Rhodnius prolixus, Triatoma maculata, Rhodnius pallescens, Panstrongylus geniculatus and Eratyrus cuspidatus. Twenty-two species were identified as blood sources, resulting in an integrated transmission network with extensive connectivity among sylvatic and domestic host species. Only TcI parasites were detected, predominantly from TcIb but TcIa was also reported. The close relatedness of T. cruzi strains further supported the lack of separate transmission cycles according to habitats or triatomine species. Triatomine microbiota varied according to species, developmental stage and T. cruzi infection. Bacterial families correlated with the presence/absence of T. cruzi were identified. In conclusion, we identified a domestic transmission cycle encompassing multiple vector species and tightly connected with sylvatic hosts in the SNSM region, rather than an isolated domestic transmission cycle. Therefore, integrated interventions targeting all vector species and their contact with humans should be considered.https://scienti.minciencias.gov.co/cvlac/visualizador/generarCurriculoCv.do?cod_rh=0001344825https://scienti.minciencias.gov.co/cvlac/visualizador/generarCurriculoCv.do?cod_rh=0000009091https://scienti.minciencias.gov.co/cvlac/visualizador/generarCurriculoCv.do?cod_rh=0000318507https://orcid.org/0000-0003-0445-5814https://orcid.org/0000-0002-8093-0544https://scienti.minciencias.gov.co/gruplac/jsp/visualiza/visualizagr.jsp?nro=00000000008981andres.rojasgu@campusucc.edu.cogabriel.parrah@ucc.edu.cojose.usmec@ucc.edu.cohttps://scholar.google.es/citations?hl=es&user=gwBokScAAAAJhttps://scholar.google.es/citations?hl=es&user=1pfSvNUAAAAJhttps://scholar.google.es/citations?hl=es&user=cU2KyT4AAAAJUniversidad Cooperativa de Colombia, Facultad de Ciencias de la Salud, Medicina, Santa MartaMedicinaSanta Martahttps://www.nature.com/articles/s41598-021-91783-2#Bib1Scientific ReportsHotez, P. J. et al. An unfolding tragedy of chagas disease in North America. PLoS Negl. Trop. Dis. 7(10), e2300. https://doi.org/10.1371/journal.pntd.0002300 (2013) (PMID: 24205411).Hotez, P. J., Bottazzi, M. E., Franco-Paredes, C., Ault, S. K. & Periago, M. R. The neglected tropical diseases of Latin America and the Caribbean: A review of disease burden and distribution and a roadmap for control and elimination. PLoS Negl. Trop. Dis. 2(9), e300. https://doi.org/10.1371/journal.pntd.0000300 (2008) (PMID: 18820747).Lee, B. Y., Bacon, K. M., Bottazzi, M. E. & Hotez, P. J. Global economic burden of Chagas disease: A computational simulation model. Lancet Infect. Dis. 13(4), 342–348. https://doi.org/10.1016/S1473-3099(13)70002-1 (2013) (PMID: 23395248).WHO. Chagas disease in Latin America: An epidemiological update based on 2010 estimates. Wkly. Epidemiol. Rec. 90(6), 33–43 (2015) (PMID: 25671846).Pena-Garcia, V. H., Gomez-Palacio, A. M., Triana-Chavez, O. & Mejia-Jaramillo, A. M. Eco-epidemiology of Chagas disease in an endemic area of Colombia: Risk factor estimation, Trypanosoma cruzi characterization and identification of blood-meal sources in bugs. Am. J. Trop. Med. Hyg. 91(6), 1116–1124. https://doi.org/10.4269/ajtmh.14-0112 (2014) (PMID: 25331808).Mejia-Jaramillo, A. M. et al. Genotyping of Trypanosoma cruzi in a hyper-endemic area of Colombia reveals an overlap among domestic and sylvatic cycles of Chagas disease. Parasit. Vectors. 7, 108. https://doi.org/10.1186/1756-3305-7-108 (2014) (PMID: 24656115).Dib, J. C., Agudelo, L. A. & Velez, I. D. Prevalencia de patologías tropicales y factores de riesgo en la comunidad indígena de Bunkwimake, Sierra Nevada de Santa Marta. DUAZARY. 3(1), 38–44 (2006).Parra-Henao, G. et al. In search of congenital Chagas disease in the Sierra Nevada de Santa Marta, Colombia. Am. J. Trop. Med. Hyg. 101(3), 482–483. https://doi.org/10.4269/ajtmh.19-0110 (2019) (PMID: 31264558).Guhl, F., Aguilera, G., Pinto, N. & Vergara, D. Actualización de la distribución geográfica y ecoepidemiología de la fauna de triatominos (Reduviidae: Triatominae) en Colombia. Biomedica. 27(Suppl 1), 143–162 (2007) (PMID: 18154255).Parra-Henao, G., Suarez-Escudero, L. C. & Gonzalez-Caro, S. Potential distribution of Chagas disease vectors (Hemiptera, Reduviidae, Triatominae) in Colombia, based on Ecological Niche Modeling. J. Trop. Med. 2016, 1439090. https://doi.org/10.1155/2016/1439090 (2016) (PMID: 28115946).Rodriguez-Mongui, E., Cantillo-Barraza, O., Prieto-Alvarado, F. E. & Cucunuba, Z. M. Heterogeneity of Trypanosoma cruzi infection rates in vectors and animal reservoirs in Colombia: A systematic review and meta-analysis. Parasit. Vectors. 12(1), 308. https://doi.org/10.1186/s13071-019-3541-5 (2019) (PMID: 31221188).Dib, J., Barnabe, C., Tibayrenc, M. & Triana, O. Incrimination of Eratyrus cuspidatus (Stal) in the transmission of Chagas’ disease by molecular epidemiology analysis of Trypanosoma cruzi isolates from a geographically restricted area in the north of Colombia. Acta Trop. 111(3), 237–242. https://doi.org/10.1016/j.actatropica.2009.05.004 (2009) (PMID: 19442641).Parra Henao, G., Angulo, V., Jaramillo, N. & Restrepo, M. Triatominos (Hemiptera: Reduviidae) de ka Sierra Nevada de Santa Marta, Colombia. Aspectos epidemiológicos, entomológicos y de distribución. Rev. CES Med. 23(1), 17–26 (2009).Hernandez, C. et al. Untangling the transmission dynamics of primary and secondary vectors of Trypanosoma cruzi in Colombia: Parasite infection, feeding sources and discrete typing units. Parasit. Vectors. 9(1), 620. https://doi.org/10.1186/s13071-016-1907-5 (2016) (PMID: 27903288).Cantillo-Barraza, O., Chaverra, D., Marcet, P., Arboleda-Sanchez, S. & Triana-Chavez, O. Trypanosoma cruzi transmission in a Colombian Caribbean region suggests that secondary vectors play an important epidemiological role. Parasit. Vectors. 7, 381. https://doi.org/10.1186/1756-3305-7-381 (2014) (PMID: 25141852).Weiss, B. & Aksoy, S. Microbiome influences on insect host vector competence. Trends Parasitol. 27(11), 514–522. https://doi.org/10.1016/j.pt.2011.05.001 (2011) (PMID: 21697014).Azambuja, P., Garcia, E. S. & Ratcliffe, N. A. Gut microbiota and parasite transmission by insect vectors. Trends Parasitol. 21(12), 568–572 (2005) (PMID: 16226491).Dumonteil, E. et al. Interactions among Triatoma sanguisuga blood feeding sources, gut microbiota and Trypanosoma cruzi diversity in southern Louisiana. Mol Ecol. 29(19), 3747–3761 (2020).Zingales, B. et al. A new consensus for Trypanosoma cruzi intraspecific nomenclature: Second revision meeting recommends TcI to TcVI. Mem. Inst. Oswaldo Cruz. 104(7), 1051–1054 (2009) (PMID: 20027478).Zingales, B. et al. The revised Trypanosoma cruzi subspecific nomenclature: Rationale, epidemiological relevance and research applications. Infect. Genet. Evol. 12(2), 240–253. https://doi.org/10.1016/j.meegid.2011.12.009 (2012) (PMID: 22226704).Tibayrenc, M. & Ayala, F. J. The population genetics of Trypanosoma cruzi revisited in the light of the predominant clonal evolution model. Acta Trop. 151, 156–165. https://doi.org/10.1016/j.actatropica.2015.05.006 (2015) (PMID: 26188332).Majeau, A., Murphy, L., Herrera, C. & Dumonteil, E. Assessing Trypanosoma cruzi parasite diversity through comparative genomics: Implications for disease epidemiology and diagnostics. Pathogens. 10, 212. https://doi.org/10.3390/pathogens10020212 (2021).Flores-Ferrer, A., Marcou, O., Waleckx, E., Dumonteil, E. & Gourbière, S. Evolutionary ecology of Chagas disease; what do we know and what do we need?. Evol. Appl. 11(4), 470–487. https://doi.org/10.1111/eva.12582 (2017).Tibayrenc, M., Kjellberg, F. & Ayala, F. J. A clonal theory of parasitic protozoa: The population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas, and Trypanosoma and their medical and taxonomical consequences. Proc. Natl. Acad. Sci. USA 87, 2414–2418 (1990).Berry, A. S. F. et al. Sexual reproduction in a natural Trypanosoma cruzi population. PLoS Negl. Trop. Dis. 13(5), e0007392. https://doi.org/10.1371/journal.pntd.0007392 (2019) (PMID: 31107905).Schwabl, P. et al. Meiotic sex in Chagas disease parasite Trypanosoma cruzi. Nat. Commun. 10(1), 3972. https://doi.org/10.1038/s41467-019-11771-z (2019) (PMID: 31481692).Falla, A. et al. Haplotype identification within Trypanosoma cruzi I in Colombian isolates from several reservoirs, vectors and humans. Acta Trop. 110(1), 15–21 (2009) (PMID: 19135020).Cura, C. I. et al. Trypanosoma cruzi I genotypes in different geographical regions and transmission cycles based on a microsatellite motif of the intergenic spacer of spliced-leader genes. Int. J. Parasitol. 40(14), 1599–1607. https://doi.org/10.1016/j.ijpara.2010.06.006 (2010) (PMID: 20670628).Rodriguez, I. B. et al. Transmission dynamics of Trypanosoma cruzi determined by low-stringency single primer polymerase chain reaction and southern blot analyses in four indigenous communities of the Sierra Nevada de Santa Marta, Colombia. Am. J. Trop. Med. Hyg. 81(3), 396–403 (2009) (PMID: 19706903).Waleckx, E., Gourbière, S. & Dumonteil, E. Intrusive triatomines and the challenge of adapting vector control practices. Mem. Inst. Oswaldo Cruz. 110(3), 324–338 (2015).Dumonteil, E. 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. 8(1), 4140. https://doi.org/10.1038/s41598-018-22455-x (2018) (PMID: 29515202).Dumonteil, E. et al. Interactions among Triatoma sanguisuga blood feeding sources, gut microbiota and Trypanosoma cruzi diversity in southern Louisiana. Mol. Ecol. https://doi.org/10.1111/mec.15582 (2020) (PMID: 32749727).O’Connor, O., Bosseno, M. F., Barnabe, C., Douzery, E. J. & Breniere, S. F. Genetic clustering of Trypanosoma cruzi I lineage evidenced by intergenic miniexon gene sequencing. Infect. Genet. Evol. 7(5), 587–593. https://doi.org/10.1016/j.meegid.2007.05.003 (2007) (PMID: 17553755).Villanueva-Lizama, L., Teh-Poot, C., Majeau, A., Herrera, C. & Dumonteil, E. Molecular genotyping of Trypanosoma cruzi by next-generation sequencing of the mini-exon gene reveals infections with multiple parasite DTUs in Chagasic patients from Yucatan, Mexico. J. Inf. Dis. 219(12), 1980–1988 (2019).Parra-Henao, G., Angulo, V. M., Osorio, L. & Jaramillo, O. N. Geographic distribution and ecology of Triatoma dimidiata (Hemiptera: Reduviidae) in Colombia. J. Med. Entomol. 53(1), 122–129. https://doi.org/10.1093/jme/tjv163 (2016) (PMID: 26487247).Angulo, V. M., Esteban, L. & Luna, K. P. Attalea butyracea proximas a las viviendas como posible fuente de infestacion domiciliaria por Rhodnius prolixus (Hemiptera: Reduviidae) en los Llanos Orientales de Colombia. Biomedica. 32(2), 277–285. https://doi.org/10.1590/S0120-41572012000300016 (2012) (PMID: 23242302).Feliciangeli, M. D., Sanchez-Martin, M., Marrero, R., Davies, C. & Dujardin, J. P. Morphometric evidence for a possible role of Rhodnius prolixus from palm trees in house re-infestation in the State of Barinas (Venezuela). Acta Trop. 101(2), 169–177. https://doi.org/10.1016/j.actatropica.2006.12.010 (2007) (PMID: 17306204).Fitzpatrick, S., Feliciangeli, M. D., Sanchez-Martin, M. J., Monteiro, F. A. & Miles, M. A. Molecular genetics reveal that silvatic Rhodnius prolixus do colonise rural houses. PLoS Negl. Trop. Dis. 2(4), e210. https://doi.org/10.1371/journal.pntd.0000210 (2008) (PMID: 18382605).Lopez, G. & Moreno, J. Genetic variability and differentiation between populations of Rhodnius prolixus and R. pallescens, vectors of Chagas’ disease in Colombia. Mem. Inst. Oswaldo Cruz. 90, 353–357 (1995).Dumonteil, E. et al. Detailed ecological associations of triatomines revealed by metabarcoding based on next-generation sequencing: linking triatomine behavioral ecology and Trypanosoma cruzi transmission cycles. Sci. Rep. 8(1), 4140. https://doi.org/10.1038/s41598-018-22455-x (2018).Hernández-Andrade, A., Moo-Millan, J., Cigarroa-Toledo, N., Ramos-Ligonio, A., Herrera, C., Bucheton, B., et al. Metabarcoding: A powerful yet still underestimated approach for the comprehensive study of vector-borne pathogen transmission cycles and their dynamics. in Vector-Borne Diseases: Recent Developments in Epidemiology and Control (ed. Claborn, D.) 1–6. (Intechopen, 2020). https://doi.org/10.5772/intechopen.83110Flores-Ferrer, A., Waleckx, E., Rascalou, G., Dumonteil, E. & Gourbière, S. Trypanosoma cruzi transmission dynamics in a synanthropic and domesticated host community. PLoS Negl. Trop. Dis. 13(12), e0007902. https://doi.org/10.1371/journal.pntd.0007902 (2019).Llewellyn, M. S. et al. Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathog. 5(5), e1000410. https://doi.org/10.1371/journal.ppat.1000410 (2009) (PMID: 19412340).Herrera, C. et al. Genetic variability and phylogenetic relationships within Trypanosoma cruzi I isolated in Colombia based on Miniexon Gene Sequences. J. Parasitol. Res. https://doi.org/10.1155/2009/897364 (2009) (PMID: 20798881).Zumaya-Estrada, F. A. et al. North American import? Charting the origins of an enigmatic Trypanosoma cruzi domestic genotype. Parasit. Vectors. 5, 226. https://doi.org/10.1186/1756-3305-5-226 (2012) (PMID: 23050833).Montoya-Porras, L. M., Omar, T. C., Alzate, J. F., Moreno-Herrera, C. X. & Cadavid-Restrepo, G. E. 16S rRNA gene amplicon sequencing reveals dominance of Actinobacteria in Rhodnius pallescens compared to Triatoma maculata midgut microbiota in natural populations of vector insects from Colombia. Acta Trop. 178, 327–332. https://doi.org/10.1016/j.actatropica.2017.11.004 (2018) (PMID: 29154947).Kieran, T. J. et al. Regional biogeography of microbiota composition in the Chagas disease vector Rhodnius pallescens. Parasit. Vectors. 12(1), 504. https://doi.org/10.1186/s13071-019-3761-8 (2019) (PMID: 31665056).Rodriguez-Ruano, S. M. et al. Microbiomes of North American Triatominae: The grounds for Chagas Disease epidemiology. Front. Microbiol. 9, 1167. https://doi.org/10.3389/fmicb.2018.01167 (2018) (PMID: 29951039).Eichler, S. & Schaub, G. A. Development of symbionts in triatomine bugs and the effects of infections with trypanosomatids. Exp. Parasitol. 100(1), 17–27 (2002).Waltmann, A. et al. Hindgut microbiota in laboratory-reared and wild Triatoma infestans. PLoS Negl. Trop. Dis. 13(5), e0007383. https://doi.org/10.1371/journal.pntd.0007383 (2019) (PMID: 31059501).Herren, J. K. et al. A microsporidian impairs Plasmodium falciparum transmission in Anopheles arabiensis mosquitoes. Nat. Commun. 11(1), 2187. https://doi.org/10.1038/s41467-020-16121-y (2020) (PMID: 32366903).Moreira, L. A. et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139(7), 1268–1278. https://doi.org/10.1016/j.cell.2009.11.042 (2009) (PMID: 20064373).Angulo, V. M. & Esteban, L. Nueva trampa para la captura de triatominos en habitats silvestres y peridomesticos. Biomedica. 31(2), 264–268. https://doi.org/10.1590/S0120-41572011000200015 (2011) (PMID: 22159544).Lent, H. & Wygodzinsky, P. Revision of Triatominae (Hemiptera: Reduviidae), and their significance as vectors of Chagas’ disease. Bull. Am. Mus. Nat. His. 163, 123–520 (1979).Monteiro, F. A. et al. Molecular phylogeography of the Amazonian Chagas disease vectors Rhodnius prolixus and R. robustus. Mol. Ecol. 12(4), 997–1006. https://doi.org/10.1046/j.1365-294x.2003.01802.x (2003) (PMID: 12753218).Baker, G. C., Smith, J. J. & Cowan, D. A. Review and reanalysis of domain-specific 16s primers. J. Microbiol. Meth. 55, 541–555 (2003).Heuer, H., Krsek, M., Baker, P., Smalla, K. & Wellington, E. M. Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl. Environ. Microbiol. 63(8), 3233–3241 (1997).Souto, R. P., Fernandes, O., Macedo, A. M., Campbell, D. A. & Zingales, B. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol. Biochem. Parasitol. 83(2), 141–152 (1996) (PMID: 9027747).Majeau, A., Herrera, C. & Dumonteil, E. An improved approach to Trypanosoma cruzi molecular genotyping by next-generation sequencing of the mini-exon gene. Methods Mol. Biol. 1955, 47–60 (2019).Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16), 2194–2200. https://doi.org/10.1093/bioinformatics/btr381 (2011) (PMID: 21700674).Garrison E, Marth G. Haplotype-based variant detection from short-read sequencing. arXiv preprint. (arXiv:1207.3907 [q-bio.GN]), 1–9. https://arxiv.org/abs/1207.3907v2 (2012).Dhariwal, A. et al. MicrobiomeAnalyst: A web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res. 45(W1), W180–W188. https://doi.org/10.1093/nar/gkx295 (2017) (PMID: 28449106).Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—Approximately maximum-likelihood trees for large alignments. PLoS ONE 5(3), e9490. https://doi.org/10.1371/journal.pone.0009490 (2010) (PMID: 20224823).Bouckaert, R. et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol. 15(4), e1006650. https://doi.org/10.1371/journal.pcbi.1006650 (2019) (PMID: 30958812).Torres-Silva, C. F. et al. Assessment of genetic mutation frequency induced by oxidative stress in Trypanosoma cruzi. Genet Mol Biol. 41(2), 466–474. https://doi.org/10.1590/1678-4685-GMB-2017-0281 (2018) (PMID: 30088612).Hammer, Ø., Harper, D. A. T. & Ryan, P. D. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4(1), 9 (2001).Cole, J. R. et al. Ribosomal Database Project: Data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42(Database issue), D633–D642. https://doi.org/10.1093/nar/gkt1244 (2014) (PMID: 24288368).Trypanosoma cruziSierra Nevada de Santa MartaDiversity and interactions among triatomine bugs, their blood feeding sources, gut microbiota and Trypanosoma cruzi in the Sierra Nevada de Santa Marta in ColombiaArtículos Científicoshttp://purl.org/coar/resource_type/c_2df8fbb1http://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionAtribucióninfo:eu-repo/semantics/openAccesshttp://purl.org/coar/access_right/c_abf2PublicationORIGINALs41598-021-91783-2.pdfs41598-021-91783-2.pdfArticuloapplication/pdf4196814https://repository.ucc.edu.co/bitstreams/43fb9e17-0d70-4161-a9e9-729f9ef36668/download65789589751335bedf8ff86cba7aaff6MD51LICENSElicense.txtlicense.txttext/plain; charset=utf-81748https://repository.ucc.edu.co/bitstreams/35144856-777f-4026-875d-f18a40825810/download8a4605be74aa9ea9d79846c1fba20a33MD52THUMBNAILs41598-021-91783-2.pdf.jpgs41598-021-91783-2.pdf.jpgGenerated Thumbnailimage/jpeg6454https://repository.ucc.edu.co/bitstreams/1c060a76-cbb1-40c6-876d-2417bf608ef9/download660e1a59cd2594a874c4e62bf73645c3MD53TEXTs41598-021-91783-2.pdf.txts41598-021-91783-2.pdf.txtExtracted texttext/plain67014https://repository.ucc.edu.co/bitstreams/fa5780c8-d2e2-4312-9c6b-dc37aab505e1/download03d8f8674bbee59e5c51dc80f8bc0789MD5420.500.12494/46838oai:repository.ucc.edu.co:20.500.12494/468382024-08-10 22:48:14.863restrictedhttps://repository.ucc.edu.coRepositorio Institucional Universidad Cooperativa de Colombiabdigital@metabiblioteca.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