Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities

Chagas disease (CHD) is the highest economic burden parasitosis worldwide and the most important cardiac infection, without therapeutic alternatives to halt or reverse its progression. In CHD-experimental models, antioxidant and anti-inflammatory compounds have demonstrated therapeutic potential in...

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Autores:
Vargas-Munévar, Laura
Borja-Fajardo, Juan
Sandoval-Aldana, Angélica
García, Wendy Quintero
Moreno, Erika Moreno
Henriquez, Juan Camilo
Stashenko, Elena
García, Liliana Torcoroma
García-Beltrán, Olimpo
Tipo de recurso:
Article of investigation
Fecha de publicación:
2024
Institución:
Universidad de Ibagué
Repositorio:
Repositorio Universidad de Ibagué
Idioma:
eng
OAI Identifier:
oai:repositorio.unibague.edu.co:20.500.12313/5907
Acceso en línea:
https://hdl.handle.net/20.500.12313/5907
https://www.sciencedirect.com/science/article/pii/S0753332224001884
Palabra clave:
Antioxidant
Chagas disease
Immunomodulator
Polyphenols
Theobroma cacao L
Trypanosoma cruzi
Rights
openAccess
License
© 2024 The Authors
id UNIBAGUE2_3232d042e348faaefe7af50a8b163222
oai_identifier_str oai:repositorio.unibague.edu.co:20.500.12313/5907
network_acronym_str UNIBAGUE2
network_name_str Repositorio Universidad de Ibagué
repository_id_str
dc.title.eng.fl_str_mv Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities
title Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities
spellingShingle Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities
Antioxidant
Chagas disease
Immunomodulator
Polyphenols
Theobroma cacao L
Trypanosoma cruzi
title_short Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities
title_full Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities
title_fullStr Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities
title_full_unstemmed Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities
title_sort Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities
dc.creator.fl_str_mv Vargas-Munévar, Laura
Borja-Fajardo, Juan
Sandoval-Aldana, Angélica
García, Wendy Quintero
Moreno, Erika Moreno
Henriquez, Juan Camilo
Stashenko, Elena
García, Liliana Torcoroma
García-Beltrán, Olimpo
dc.contributor.author.none.fl_str_mv Vargas-Munévar, Laura
Borja-Fajardo, Juan
Sandoval-Aldana, Angélica
García, Wendy Quintero
Moreno, Erika Moreno
Henriquez, Juan Camilo
Stashenko, Elena
García, Liliana Torcoroma
García-Beltrán, Olimpo
dc.subject.proposal.eng.fl_str_mv Antioxidant
Chagas disease
Immunomodulator
Polyphenols
Theobroma cacao L
Trypanosoma cruzi
topic Antioxidant
Chagas disease
Immunomodulator
Polyphenols
Theobroma cacao L
Trypanosoma cruzi
description Chagas disease (CHD) is the highest economic burden parasitosis worldwide and the most important cardiac infection, without therapeutic alternatives to halt or reverse its progression. In CHD-experimental models, antioxidant and anti-inflammatory compounds have demonstrated therapeutic potential in cardiac dysfunction. Theobroma cacao polyphenols are potent natural antioxidants with cardioprotective and anti-inflammatory action, which are susceptible to degradation, requiring technological approaches to guarantee their protection, stability, and controlled release. Here, 21 cocoa polyphenol-rich microencapsulates were produced by spray-drying and freeze-drying techniques using two wall materials (maltodextrin and gum arabic). Chemical (total and individual phenolic content and antioxidant activity), structural (morphology), and biological parameters (cytotoxicity, trypanocidal, antioxidant, and immunomodulatory activities) were assessed to determine the most efficient microencapsulation conditions on Trypanosoma cruzi-infected myocardioblast and macrophage cells. Significant antiproliferative properties against infected cells (superior to benznidazole) were found in two microencapsulates which also exhibited cardioprotective properties against oxidative stress, inflammation, and cell death.
publishDate 2024
dc.date.issued.none.fl_str_mv 2024-04
dc.date.accessioned.none.fl_str_mv 2025-11-06T19:18:26Z
dc.date.available.none.fl_str_mv 2025-11-06T19:18:26Z
dc.type.none.fl_str_mv Artículo de revista
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
dc.type.content.none.fl_str_mv Text
dc.type.driver.none.fl_str_mv info:eu-repo/semantics/article
dc.type.version.none.fl_str_mv info:eu-repo/semantics/publishedVersion
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dc.identifier.citation.none.fl_str_mv Vargas-Munévar, L., Borja-Fajardo, J., Sandoval-Aldana, A., García, W., Moreno, E., Henriquez, J., Stashenko, E., García, L. y García-Beltrán, O. (2024). Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities. Biomedicine and Pharmacotherapy, 173. DOI: 10.1016/j.biopha.2024.116307
dc.identifier.doi.none.fl_str_mv DOI: 10.1016/j.biopha.2024.116307
dc.identifier.eissn.none.fl_str_mv 19506007
dc.identifier.issn.none.fl_str_mv 07533322
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12313/5907
dc.identifier.url.none.fl_str_mv https://www.sciencedirect.com/science/article/pii/S0753332224001884
identifier_str_mv Vargas-Munévar, L., Borja-Fajardo, J., Sandoval-Aldana, A., García, W., Moreno, E., Henriquez, J., Stashenko, E., García, L. y García-Beltrán, O. (2024). Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities. Biomedicine and Pharmacotherapy, 173. DOI: 10.1016/j.biopha.2024.116307
DOI: 10.1016/j.biopha.2024.116307
19506007
07533322
url https://hdl.handle.net/20.500.12313/5907
https://www.sciencedirect.com/science/article/pii/S0753332224001884
dc.language.iso.none.fl_str_mv eng
language eng
dc.relation.citationvolume.none.fl_str_mv 173
dc.relation.ispartofjournal.none.fl_str_mv Biomedicine and Pharmacotherapy
dc.relation.references.none.fl_str_mv K.M. Bonney, Chagas disease in the 21st Century: a public health success or an emerging threat ? Parasite 21 (2014) 11, https://doi.org/10.1051/parasite/ 201401
K.C.F. Lidani, F.A. Andrade, L. Bavia, F.S. Damasceno, M.H. Beltrame, I.J. MessiasReason, T.L. Sandri, Chagas disease: from discovery to a worldwide health problem, Front. Public Heal. 7 (2019) 166, https://doi.org/10.3389/ fpubh.2019.00166
J.D. Whitman, Clinical microbiology, Clin. Microbiol. Newsl. 45 (2023) 141–149, https://doi.org/10.1016/j.clinmicnews.2023.09.001.
B.Y. Lee, K.M. Bacon, M.E. Bottazzi, P.J. Hotez, Global economic burden of Chagas disease: a computational simulation model, Lancet Infect. Dis. 13 (2013) 342–348, https://doi.org/10.1016/S1473-3099(13)70002-1
K.M. Bonney, D.J. Luthringer, S.A. Kim, N.J. Garg, D.M. Engman, Pathology and pathogenesis of Chagas heart disease, Annu Rev. Pathol. 14 (2019) 421–447, https://doi.org/10.1146/annurev-pathol-020117-043711.
A.C. Cristovao-Silva, ˜ M.C.A. Brelaz-de-Castro, M.Z. Hernandes, V.R.A. Pereira, Chagas disease: immunology of the disease at a glance, Cytokine Growth Factor Rev. 62 (2021) 15–22, https://doi.org/10.1016/j.cytogfr.2021.10.001
E. Maldonado, D.A. Rojas, F. Urbina, A. Solari, Review article the oxidative stress and chronic inflammatory process in Chagas disease: role of exosomes and contributing genetic factors, Oxid. Med. Cell. Longev. 2021 (2021), https://doi. org/10.1155/2021/4993452
F. Lascano, F.G. Bournissen, J. Altcheh, Review of pharmacological options for the treatment of Chagas disease, Br. J. Clin. Pharmacol. 88 (2022) 383–402, https:// doi.org/10.1111/bcp.14
D.X. Espinel-Mesa, C.I. Gonz´ alez-Rugeles, J.C. Mantilla-Hern´ andez, E.E. Stashenko, C.A. Villegas-Lanau, J.J. Quimbaya-Ramírez, L.T. García-Sanchez, ´ Immunomodulation and antioxidant activities as possible trypanocidal and cardioprotective mechanisms of major terpenes from Lippia alba Essential oils in an experimental model of chronic Chagas disease, Antioxidants 10 (2021) 1851, https://doi.org/10.3390/antiox10111851.
M.C. Montenote, V.Z. Wajsman, Y.T. Konno, P.C. Ferreira, R.M.G. Silva, A.L. S. Therezo, L.P.A. Martins, Antioxidant effect of Morus nigra on Chagas disease progression, Rev. Inst. Med. Trop. Sao Paulo 59 (2017) 1–11, https://doi.org/ 10.1590/S1678-9946201759073
R.D. Novaes, M.V.P. Sartini, J.P.F. Rodrigues, R.V. Gonçalves, E.C. Santos, R.L. M. Souza, I.S. Caldas, Curcumin enhances the anti- Trypanosoma cruzi activity of benznidazole-based chemotherapy in acute experimental Chagas disease, Antimicrob. Agents Chemother. 60 (2016) 3355–3364, https://doi.org/10.1128/ AAC.00343-16.
C. Paveto, M.C. Gu, I. Esteva, V. Martino, J. Coussio, M.M. Flawia, AntiTrypanosoma cruzi activity of green tea (Camellia sinensis) catechins, Antimicrob. Agents Chemother. 48 (2004) 69–74, https://doi.org/10.1128/AAC.48.1.69.
ICCO. International Cacao Organization. Available online: 〈https://www.icco. org/aboutcac
FEDECACAO. Federacion ´ Nacional de Cacaoteros. El Cacaocultor es lo Primero. Economía Internacional. Available online: 〈https://www.fedecacao.com.co/port al/index.php/es/2015-02-12-17-20-59/nacionales〉 (Access
EFSA, Panel on dietetic products, nutrition and allergies (NDA). Scientific opinion on the substantiation of a health claim related to cocoa flavanols and maintenance of normal endothelium-dependent vasodilation pursuant to Article 13 (5) of Regulation (EC) No 1924/2006, EFSA J. 10 (2012) 2809, https://doi.org/10.2903/ j.efsa.2012.2809.
Y. Rodríguez-Carrasco, A. Gaspari, G. Graziani, A. Santini, A. Ritieni, Fast analysis of polyphenols and alkaloids in cocoa-based products by ultra-high performance liquid chromatography and Orbitrap high resolution mass spectrometry (UHPLCQ-Orbitrap-MS/MS), Int. Food Res. J. 111 (2018) 229–236, https://doi.org/ 10.1016/j.foodres.2018.05.03
L. Dugo, G. Tripodo, L. Santi, C. Fanali, Cocoa polyphenols: chemistry, bioavailability and effects on cardiovascular performance, Curr. Med. Chem. 25 (2018) 4903–4917, https://doi.org/10.2174/0929867323666160919094339.
D.L. Katz, K. Doughty, A. Ali, Cocoa and chocolate in human health and disease, Antioxid. Redox Signal 15 (2011) 2779–2811, https://doi.org/10.1089/ ars.2010.3697.
O. Yanez, ˜ M.I. Osorio, C. Areche, A. Vasquez-Espinal, J. Bravo, A. SandovalAldana, W. Tiznado, Theobroma cacao L. compounds: theoretical study and molecular modeling as inhibitors of main SARS-CoV-2 protease, Biomed. Pharm. 140 (2021) 111764, https://doi.org/10.1016/j.biopha.2021.111764.
J. Wollgast, E. Anklam, Review on polyphenols in Theobroma cacao: changes in composition during the manufacture of chocolate and methodology for identi ® cation and quanti ® cation, Int. Food Res. J. 33 (2000) 423–447, https://doi.org/ 10.1016/S0963-9969(00)00068-5.
L. Dugo, M.G. Belluomo, C. Fanali, M. Russo, F. Cacciola, M. Maccarrone, A. M. Sardanelli, Effect of cocoa polyphenolic extract on macrophage polarization from proinflammatory M1 to anti-inflammatory M2 state, Oxid. Med. Cell Longe 2017 (2017), https://doi.org/10.1155/2017/6293740
Q.R. Araujo, Gattward De, J.N. Almoosawi, S. Conceiç˜ ao, G. Costa, P. Santana, P. A. De, G. Conceiç˜ ao, P. Costa, P. Alfredo, D.S. Dantas, et al., Cocoa and human health: from head to foot - a review, Crit. Rev. Food Sci. Nutr. 56 (2016) 1–12, https://doi.org/10.1080/10408398.2012.657921.
S.A. Oyeleke, A.M. Ajayi, S. Umukoro, A.O. Aderibigbe, O.G. Ademowo, Antiinflammatory activity of Theobroma cacao L. stem bark ethanol extract and its fractions in experimental models, J. Ethnopharmacol. 222 (2018) 239–248, https://doi.org/10.1016/j.jep.2018.04.050
N. Sari, Y. Katanasaka, H. Honda, Y. Miyazaki, Y. Sunagawa, M. Funamoto, T. Morimoto, Cacao bean polyphenols inhibit cardiac hypertrophy and systolic dysfunction in pressure overload-induced heart failure model mice, Planta Med. 86 (2020) 1304–1312, https://doi.org/10.1055/a-1191-7970.
J.W. Li, X.Y. Wang, X. Zhang, L. Gao, L.F. Wang, X.H. Yin, -)-Epicatechin protects against myocardial ischemia-induced cardiac injury via activation of the PTEN/ PI3K/AKT pathway, Mol. Med. Rep. 17 (2018) 8300–8308, https://doi.org/ 10.3892/mmr.2018.8870
H.D. Sesso, J.E. Manson, A.K. Aragaki, P.M. Rist, L.G. Johnson, G. Friedenberg, G. L. Anderson, Effect of cocoa flavanol supplementation for the prevention of cardiovascular disease events: the cocoa supplement and multivitamin outcomes study (COSMOS) randomized clinical trial, Am. J. Clin. Nutr. 115 (2022) 1490–1500, https://doi.org/10.1093/ajcn/nqac055.
M. Darand, M. Hajizadeh-Oghaz, A. Hadi, M. Atefi, R. Amani, The effect of cocoa/ dark chocolate consumption on lipid profile, glycemia, and blood pressure in diabetic patients: a meta-analysis of observational studies, Phytother. Res. 35 (2021) 5487–5501, https://doi.org/10.1002/ptr.7183.
P. Vitaglione, R. Barone Lumaga, R. Ferracane, S. Sellitto, J.R. Morello, ´ J. Reguant Miranda, E. Shimoni, V. Fogliano, Human bioavailability of flavanols and phenolic acids from cocoa-nut creams enriched with free or microencapsulated cocoa polyphenols, Br. J. Nutr. 109 (2013) 1832–1843, https://doi.org/10.1017/ S0007114512003881
L.F. Ballesteros, M.J. Ramirez, C.E. Orrego, J.A. Teixeira, S.I. Mussatto, Encapsulation of antioxidant phenolic compounds extracted from spent coffee grounds by freeze-drying and spray-drying using different coating materials, Food Chem. 237 (2017) 623–631, https://doi.org/10.1016/j.foodchem.2017.05.142
Z. Jiang, Z. Han, M. Zhu, X. Wan, L. Zhang, Effects of thermal processing on transformation of polyphenols and flavor quality, Curr. Opin. Food Sci. 51 (2023) 101014, https://doi.org/10.1016/j.cofs.2023.101014.
V.L. Singleton, R. Orthofer, R.M. Lamuela-Raventos, ´ Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent, Methods Enzym. 299 (1999) 152–178, https://doi.org/10.1016/S0076-6879(99) 99017-1
I.F.F. Benzie, J.J. Strain, The ferric reducing ability of plasma ( FRAP) as a measure of "antioxidant power", FRAP Assay. 239 (1996) 70–76, https://doi.org/10.1006/ abio.1996.029
W. Brand-Williams, M.E. Cuvelier, C.L.W.T. Berset, Use of a free radical method to evaluate antioxidant activity, LWT Food Sci. Techno 28 (1995) 25–30, https://doi. org/10.1016/S0023-6438(95)80008-5
B. Ou, M. Hampsch-woodill, R.L. Prior, Development and validation of an improved oxygen radical absorbance capacity assay using fluorescein as the fluorescent probe, J. Agric. Food Chem. 49 (2001) 4619–4626, https://doi.org/ 10.1021/jf010586
W.L. Quintero, E.M. Moreno, S. Milena, L. Pinto, S.M. Sanabria, E. Stashenko, L. T. García, Immunomodulatory, trypanocide, and antioxidant properties of essential oil fractions of Lippia alba ( Verbenaceae), BMC Complement Altern. Med. 21 (1) (2021) 16, https://doi.org/10.1186/s12906-021-03347-6.
L.C. Carrillo, J. Londono-Londo ˜ no, ˜ A. Gil, Comparison of polyphenol, methylxanthines and antioxidant activity in Theobroma cacao beans from different cocoa-growing areas in Colombia, FRIN 60 (2014) 273–280, https://doi.org/ 10.1016/j.foodres.2013.06.01
S. Kandasamy, R. Naveen, A review on the encapsulation of bioactive components using spray-drying and freeze-drying techniques, J. Food Process Eng. 45 (2022) 1–14, https://doi.org/10.1111/jfpe.14059.
M.J. Payne, W.J. Hurst, K.B. Miller, C. Rank, D.A. Stuart, Impact of fermentation, drying, roasting, and dutch processing on epicatechin and catechin content of cacao beans and cocoa ingredients, J. Agric. Food Chem. 58 (2010) 10518–10527, https://doi.org/10.1021/jf102391q
G.E. Adamson, S.A. Lazarus, A.E. Mitchell, R.L. Prior, G. Cao, P.H. Jacobs, B. G. Kremers, J.F. Hammerstone, R.B. Rucker, K.A. Ritter, H.H. Schmitz, HPLC method for the quantification of procyanidins in cocoa and chocolate samples and correlation to total antioxidant capacity, J. Agric. Food Chem. 47 (1999) 4184–4188, https://doi.org/10.1021/jf990317m.
S. Vertuani, E. Scalambra, T. Vittorio, A. Bino, A. Baldisserotto, S. Manfredini, Evaluation of antiradical activity of different cocoa and chocolate products: relation with lipid and protein composition, J. Med. Food 17 (2014) 512–516, https://doi.org/10.1089/jmf.2013.0110.
V. Todorovic, I.R. Redovnikovic, Z. Todorovic, G. Jankovic, M. Dodevska, S. Sobajic, Polyphenols, methylxanthines, and antioxidant capacity of chocolate produced in Serbia, J. Food Compost Anal. 41 (2015) 137–143, https://doi.org/ 10.1016/j.jfca.2015.01.018
S. Zapata-Bustamante, A. Tamayo-Tenorio, B. Alberto-Rojano, Efecto de la fermentacion ´ sobre la actividad antioxidante de diferentes clones de cacao colombiano, Rev. Cuba Plantas Med. 18 (2013) 391–404.
L.J. Giraldo-Lopez, ´ Impact of fermentation and drying in polyphenol content and antioxidant capacity of cocoa variety CCN51, Rev. ION 29 (2016) 7–21, https:// doi.org/10.18273/revion.v29n2-2016001
] D.B. Haytowitz, S.U.S.D.A. Bhagwat, Database for the Oxygen Radical Absorbance Capacity (ORAC) of Selected, Foods, Release 2 3 (2010) 10–48.
A. Ricci, J.A. Arboleda, A. Versari, E. Chiarello, A. Bordoni, G.P. Parpinello, Microencapsulation of polyphenolic compounds recovered from red wine lees: process optimization and nutraceutical study, Food Bioprod. Process. 132 (2021) 1–12, https://doi.org/10.1016/j.fbp.2021.12.003
F. Felice, A. Fabiano, M. De-Leo, A.M. Piras, D. Beconcini, M.M. Cesare, A. Braca, Y. Zambito, R. Di Stefano, Antioxidant effect of cocoa by-product and cherry polyphenol extracts: a comparative study, Antioxidants 9 (2020) 1–14, https://doi. org/10.3390/antiox9020132
T.K. Kim, J.M. Hong, K.H. Kim, S.J. Han, I.C. Kim, H. Oh, J.H. Yim, Potential of ramalin and its derivatives for the treatment of alzheimer’s disease, Molecules 26 (2021) 1–12, https://doi.org/10.3390/molecules26216445.
M.J. TallonAuthorised EU health claim for cocoa flavanols. Elsevier Ltd.,2015, ISBN 9781782423829..
Z. Fang, B. Bhandari, Spray drying, freeze drying and related processes for food ingredient and nutraceutical encapsulation, ESI (2012) 73–109, https://doi.org/ 10.1533/9780857095909
G. Ferreira, F. Matta, R. Augustus, D. Oliveira, Incorporation of spray dried and freeze dried blackberry particles in edible films: morphology, stability to pH, sterilization and biodegradation, Food Packag Shelf Life 20 (2019) 100313, https://doi.org/10.1016/j.fpsl.2019.100313.
S. Krishnan, A.C. Kshirsagar, R.S. Singhal, The use of gum arabic and modified starch in the microencapsulation of a food flavoring agent, Carbohydr. Polym. 62 (2005) 309–315, https://doi.org/10.1016/j.carbpol.2005.03.020.
R. Argüello-García, G.N. Quinonez-Bastidas, ˜ Catechins as emerging and promising antiparasitic agents, Biomed. J. Sci. Technol. Res. 30 (2020) 23065–23071, https://doi.org/10.26717/BJSTR.2020.30.004895.
V. Bolanos, ˜ A. Díaz-Martínez, J. Soto, M.A. Rodríguez, C. Lopez-Camarillo, ´ L. A. Marchat, E. Ramírez-Moreno, The flavonoid (− )-epicatechin affects cytoskeleton proteins and functions in Entamoeba histolytica. J. Proteom. 111 (2014) 74–85, https://doi.org/10.1016/j.jprot.2014.05.017.
M.B.G. Dos Reis, L.C. Manjolin, C.D.C. Maquiaveli, O.A. Santos-Filho, E.R. Da Silva, Inhibition of Leishmania (Leishmania) amazonensis and rat arginases by green tea EGCG,(+)-catechin and (− )-epicatechin: a comparative structural analysis of enzyme-inhibitor interactions, PLoS One 8 (2013) e78387, https://doi.org/ 10.1371/journal.pone.007
J. Luo, H. Si, Z. Jia, D. Liu, Dietary anti-aging polyphenols and potential mechanisms, Antioxidants 10 (2021) 283, https://doi.org/10.3390/ antiox10020283.
I. Bernatova, Biological activities of (− )-epicatechin and (− )-epicatechincontaining foods: Focus on cardiovascular and neuropsychological health, Biotechnol. Adv. 36 (2018) 666–681, https://doi.org/10.1016/j. biotechadv.2
J. Oracz, E. Nebesny, D. Zyzelewicz, G. Budryn, B. Luzak, Bioavailability and metabolism of selected cocoa bioactive compounds: a comprehensive review, Crit. Rev. Food Sci. Nutr. 60 (2020) 1947–1985, https://doi.org/10.1080/ 10408398.2019.161916
F.A. Tomas-Barberan, ´ E. Cienfuegos-Jovellanos, A. Marín, B. Muguerza, A. GilIzquierdo, B. Cerd´ a, J.C. Espín, A new process to develop a cocoa powder with higher flavonoid monomer content and enhanced bioavailability in healthy humans, J. Agric. Food Chem. 55 (2007) 3926–3935, https://doi.org/10.1021/ jf070121
A.C. Aprotosoaie, A. Miron, A. Trifan, V.S. Luca, I.I. Costache, The cardiovascular effects of cocoa polyphenols -an overview, Diseases 4 (2016) 39, https://doi.org/ 10.3390/diseases40400
H. Schroeter, C.L. Keen, H.D. Sesso, J.E. Manson, J.R. Lupton, Is this the end of (-)-epicatechin, or not? New study highlights the complex challenges associated with research into the cardiovascular health benefits of bioactive food constituents, Am. J. Clin. Nutr. 102 (2015) 975–976, https://doi.org/10.3945/ajcn.115.117283.
E.A. Decker, Phenolics: prooxidants or antioxidants? Nutr. Rev. 55 (1997) 396–398, https://doi.org/10.1111/j.1753-4887.1997.tb01580.x.
M. Hu, B. Wu, Z. Liu, Bioavailability of polyphenols and flavonoids in the era of precision medicine, Mol. Pharm. 14 (2017) 2861–2863, https://doi.org/10.1021/ acs.molpharmaceut.7b005
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dc.publisher.none.fl_str_mv Elsevier Masson s.r.l.
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publisher.none.fl_str_mv Elsevier Masson s.r.l.
institution Universidad de Ibagué
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spelling Vargas-Munévar, Laura772a3991-0e74-4ce0-b936-6449df375bf2-1Borja-Fajardo, Juan70a9cfa7-8033-42d5-b411-b6e1dfd4818e-1Sandoval-Aldana, Angélica451da309-643e-45e3-ad8a-df8c9c2db99d-1García, Wendy Quintero88d98c9e-3547-43c5-b648-93211db69725-1Moreno, Erika Morenoc78aa325-0510-4f33-aa44-02bf89689ee0-1Henriquez, Juan Camilo01fbfe58-8cfd-4759-bf83-9a73ba9f4446-1Stashenko, Elena94c2a37e-7a64-4166-86cb-5bdd226462f9-1García, Liliana Torcoroma8671a57a-316b-4841-8cd9-3dad6c47aaa6-1García-Beltrán, Olimpo5bc12f58-2b62-4c7c-a477-0820b4de72e9-12025-11-06T19:18:26Z2025-11-06T19:18:26Z2024-04Chagas disease (CHD) is the highest economic burden parasitosis worldwide and the most important cardiac infection, without therapeutic alternatives to halt or reverse its progression. In CHD-experimental models, antioxidant and anti-inflammatory compounds have demonstrated therapeutic potential in cardiac dysfunction. Theobroma cacao polyphenols are potent natural antioxidants with cardioprotective and anti-inflammatory action, which are susceptible to degradation, requiring technological approaches to guarantee their protection, stability, and controlled release. Here, 21 cocoa polyphenol-rich microencapsulates were produced by spray-drying and freeze-drying techniques using two wall materials (maltodextrin and gum arabic). Chemical (total and individual phenolic content and antioxidant activity), structural (morphology), and biological parameters (cytotoxicity, trypanocidal, antioxidant, and immunomodulatory activities) were assessed to determine the most efficient microencapsulation conditions on Trypanosoma cruzi-infected myocardioblast and macrophage cells. Significant antiproliferative properties against infected cells (superior to benznidazole) were found in two microencapsulates which also exhibited cardioprotective properties against oxidative stress, inflammation, and cell death.application/pdfVargas-Munévar, L., Borja-Fajardo, J., Sandoval-Aldana, A., García, W., Moreno, E., Henriquez, J., Stashenko, E., García, L. y García-Beltrán, O. (2024). Microencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activities. Biomedicine and Pharmacotherapy, 173. DOI: 10.1016/j.biopha.2024.116307DOI: 10.1016/j.biopha.2024.1163071950600707533322https://hdl.handle.net/20.500.12313/5907https://www.sciencedirect.com/science/article/pii/S0753332224001884engElsevier Masson s.r.l.Francia173Biomedicine and PharmacotherapyK.M. Bonney, Chagas disease in the 21st Century: a public health success or an emerging threat ? Parasite 21 (2014) 11, https://doi.org/10.1051/parasite/ 201401K.C.F. Lidani, F.A. Andrade, L. Bavia, F.S. Damasceno, M.H. Beltrame, I.J. MessiasReason, T.L. Sandri, Chagas disease: from discovery to a worldwide health problem, Front. Public Heal. 7 (2019) 166, https://doi.org/10.3389/ fpubh.2019.00166J.D. Whitman, Clinical microbiology, Clin. Microbiol. Newsl. 45 (2023) 141–149, https://doi.org/10.1016/j.clinmicnews.2023.09.001.B.Y. Lee, K.M. Bacon, M.E. Bottazzi, P.J. Hotez, Global economic burden of Chagas disease: a computational simulation model, Lancet Infect. Dis. 13 (2013) 342–348, https://doi.org/10.1016/S1473-3099(13)70002-1K.M. Bonney, D.J. Luthringer, S.A. Kim, N.J. Garg, D.M. Engman, Pathology and pathogenesis of Chagas heart disease, Annu Rev. Pathol. 14 (2019) 421–447, https://doi.org/10.1146/annurev-pathol-020117-043711.A.C. Cristovao-Silva, ˜ M.C.A. Brelaz-de-Castro, M.Z. Hernandes, V.R.A. Pereira, Chagas disease: immunology of the disease at a glance, Cytokine Growth Factor Rev. 62 (2021) 15–22, https://doi.org/10.1016/j.cytogfr.2021.10.001E. Maldonado, D.A. Rojas, F. Urbina, A. Solari, Review article the oxidative stress and chronic inflammatory process in Chagas disease: role of exosomes and contributing genetic factors, Oxid. Med. Cell. Longev. 2021 (2021), https://doi. org/10.1155/2021/4993452F. Lascano, F.G. Bournissen, J. Altcheh, Review of pharmacological options for the treatment of Chagas disease, Br. J. Clin. Pharmacol. 88 (2022) 383–402, https:// doi.org/10.1111/bcp.14D.X. Espinel-Mesa, C.I. Gonz´ alez-Rugeles, J.C. Mantilla-Hern´ andez, E.E. Stashenko, C.A. Villegas-Lanau, J.J. Quimbaya-Ramírez, L.T. García-Sanchez, ´ Immunomodulation and antioxidant activities as possible trypanocidal and cardioprotective mechanisms of major terpenes from Lippia alba Essential oils in an experimental model of chronic Chagas disease, Antioxidants 10 (2021) 1851, https://doi.org/10.3390/antiox10111851.M.C. Montenote, V.Z. Wajsman, Y.T. Konno, P.C. Ferreira, R.M.G. Silva, A.L. S. Therezo, L.P.A. Martins, Antioxidant effect of Morus nigra on Chagas disease progression, Rev. Inst. Med. Trop. Sao Paulo 59 (2017) 1–11, https://doi.org/ 10.1590/S1678-9946201759073R.D. Novaes, M.V.P. Sartini, J.P.F. Rodrigues, R.V. Gonçalves, E.C. Santos, R.L. M. Souza, I.S. Caldas, Curcumin enhances the anti- Trypanosoma cruzi activity of benznidazole-based chemotherapy in acute experimental Chagas disease, Antimicrob. Agents Chemother. 60 (2016) 3355–3364, https://doi.org/10.1128/ AAC.00343-16.C. Paveto, M.C. Gu, I. Esteva, V. Martino, J. Coussio, M.M. Flawia, AntiTrypanosoma cruzi activity of green tea (Camellia sinensis) catechins, Antimicrob. Agents Chemother. 48 (2004) 69–74, https://doi.org/10.1128/AAC.48.1.69.ICCO. International Cacao Organization. Available online: 〈https://www.icco. org/aboutcacFEDECACAO. Federacion ´ Nacional de Cacaoteros. El Cacaocultor es lo Primero. Economía Internacional. Available online: 〈https://www.fedecacao.com.co/port al/index.php/es/2015-02-12-17-20-59/nacionales〉 (AccessEFSA, Panel on dietetic products, nutrition and allergies (NDA). Scientific opinion on the substantiation of a health claim related to cocoa flavanols and maintenance of normal endothelium-dependent vasodilation pursuant to Article 13 (5) of Regulation (EC) No 1924/2006, EFSA J. 10 (2012) 2809, https://doi.org/10.2903/ j.efsa.2012.2809.Y. Rodríguez-Carrasco, A. Gaspari, G. Graziani, A. Santini, A. Ritieni, Fast analysis of polyphenols and alkaloids in cocoa-based products by ultra-high performance liquid chromatography and Orbitrap high resolution mass spectrometry (UHPLCQ-Orbitrap-MS/MS), Int. Food Res. J. 111 (2018) 229–236, https://doi.org/ 10.1016/j.foodres.2018.05.03L. Dugo, G. Tripodo, L. Santi, C. Fanali, Cocoa polyphenols: chemistry, bioavailability and effects on cardiovascular performance, Curr. Med. Chem. 25 (2018) 4903–4917, https://doi.org/10.2174/0929867323666160919094339.D.L. Katz, K. Doughty, A. Ali, Cocoa and chocolate in human health and disease, Antioxid. Redox Signal 15 (2011) 2779–2811, https://doi.org/10.1089/ ars.2010.3697.O. Yanez, ˜ M.I. Osorio, C. Areche, A. Vasquez-Espinal, J. Bravo, A. SandovalAldana, W. Tiznado, Theobroma cacao L. compounds: theoretical study and molecular modeling as inhibitors of main SARS-CoV-2 protease, Biomed. Pharm. 140 (2021) 111764, https://doi.org/10.1016/j.biopha.2021.111764.J. Wollgast, E. Anklam, Review on polyphenols in Theobroma cacao: changes in composition during the manufacture of chocolate and methodology for identi ® cation and quanti ® cation, Int. Food Res. J. 33 (2000) 423–447, https://doi.org/ 10.1016/S0963-9969(00)00068-5.L. Dugo, M.G. Belluomo, C. Fanali, M. Russo, F. Cacciola, M. Maccarrone, A. M. Sardanelli, Effect of cocoa polyphenolic extract on macrophage polarization from proinflammatory M1 to anti-inflammatory M2 state, Oxid. Med. Cell Longe 2017 (2017), https://doi.org/10.1155/2017/6293740Q.R. Araujo, Gattward De, J.N. Almoosawi, S. Conceiç˜ ao, G. Costa, P. Santana, P. A. De, G. Conceiç˜ ao, P. Costa, P. Alfredo, D.S. Dantas, et al., Cocoa and human health: from head to foot - a review, Crit. Rev. Food Sci. Nutr. 56 (2016) 1–12, https://doi.org/10.1080/10408398.2012.657921.S.A. Oyeleke, A.M. Ajayi, S. Umukoro, A.O. Aderibigbe, O.G. Ademowo, Antiinflammatory activity of Theobroma cacao L. stem bark ethanol extract and its fractions in experimental models, J. Ethnopharmacol. 222 (2018) 239–248, https://doi.org/10.1016/j.jep.2018.04.050N. Sari, Y. Katanasaka, H. Honda, Y. Miyazaki, Y. Sunagawa, M. Funamoto, T. Morimoto, Cacao bean polyphenols inhibit cardiac hypertrophy and systolic dysfunction in pressure overload-induced heart failure model mice, Planta Med. 86 (2020) 1304–1312, https://doi.org/10.1055/a-1191-7970.J.W. Li, X.Y. Wang, X. Zhang, L. Gao, L.F. Wang, X.H. Yin, -)-Epicatechin protects against myocardial ischemia-induced cardiac injury via activation of the PTEN/ PI3K/AKT pathway, Mol. Med. Rep. 17 (2018) 8300–8308, https://doi.org/ 10.3892/mmr.2018.8870H.D. Sesso, J.E. Manson, A.K. Aragaki, P.M. Rist, L.G. Johnson, G. Friedenberg, G. L. Anderson, Effect of cocoa flavanol supplementation for the prevention of cardiovascular disease events: the cocoa supplement and multivitamin outcomes study (COSMOS) randomized clinical trial, Am. J. Clin. Nutr. 115 (2022) 1490–1500, https://doi.org/10.1093/ajcn/nqac055.M. Darand, M. Hajizadeh-Oghaz, A. Hadi, M. Atefi, R. Amani, The effect of cocoa/ dark chocolate consumption on lipid profile, glycemia, and blood pressure in diabetic patients: a meta-analysis of observational studies, Phytother. Res. 35 (2021) 5487–5501, https://doi.org/10.1002/ptr.7183.P. Vitaglione, R. Barone Lumaga, R. Ferracane, S. Sellitto, J.R. Morello, ´ J. Reguant Miranda, E. Shimoni, V. Fogliano, Human bioavailability of flavanols and phenolic acids from cocoa-nut creams enriched with free or microencapsulated cocoa polyphenols, Br. J. Nutr. 109 (2013) 1832–1843, https://doi.org/10.1017/ S0007114512003881L.F. Ballesteros, M.J. Ramirez, C.E. Orrego, J.A. Teixeira, S.I. Mussatto, Encapsulation of antioxidant phenolic compounds extracted from spent coffee grounds by freeze-drying and spray-drying using different coating materials, Food Chem. 237 (2017) 623–631, https://doi.org/10.1016/j.foodchem.2017.05.142Z. Jiang, Z. Han, M. Zhu, X. Wan, L. Zhang, Effects of thermal processing on transformation of polyphenols and flavor quality, Curr. Opin. Food Sci. 51 (2023) 101014, https://doi.org/10.1016/j.cofs.2023.101014.V.L. Singleton, R. Orthofer, R.M. Lamuela-Raventos, ´ Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent, Methods Enzym. 299 (1999) 152–178, https://doi.org/10.1016/S0076-6879(99) 99017-1I.F.F. Benzie, J.J. Strain, The ferric reducing ability of plasma ( FRAP) as a measure of "antioxidant power", FRAP Assay. 239 (1996) 70–76, https://doi.org/10.1006/ abio.1996.029W. Brand-Williams, M.E. Cuvelier, C.L.W.T. Berset, Use of a free radical method to evaluate antioxidant activity, LWT Food Sci. Techno 28 (1995) 25–30, https://doi. org/10.1016/S0023-6438(95)80008-5B. Ou, M. Hampsch-woodill, R.L. Prior, Development and validation of an improved oxygen radical absorbance capacity assay using fluorescein as the fluorescent probe, J. Agric. Food Chem. 49 (2001) 4619–4626, https://doi.org/ 10.1021/jf010586W.L. Quintero, E.M. Moreno, S. Milena, L. Pinto, S.M. Sanabria, E. Stashenko, L. T. García, Immunomodulatory, trypanocide, and antioxidant properties of essential oil fractions of Lippia alba ( Verbenaceae), BMC Complement Altern. Med. 21 (1) (2021) 16, https://doi.org/10.1186/s12906-021-03347-6.L.C. Carrillo, J. Londono-Londo ˜ no, ˜ A. Gil, Comparison of polyphenol, methylxanthines and antioxidant activity in Theobroma cacao beans from different cocoa-growing areas in Colombia, FRIN 60 (2014) 273–280, https://doi.org/ 10.1016/j.foodres.2013.06.01S. Kandasamy, R. Naveen, A review on the encapsulation of bioactive components using spray-drying and freeze-drying techniques, J. Food Process Eng. 45 (2022) 1–14, https://doi.org/10.1111/jfpe.14059.M.J. Payne, W.J. Hurst, K.B. Miller, C. Rank, D.A. Stuart, Impact of fermentation, drying, roasting, and dutch processing on epicatechin and catechin content of cacao beans and cocoa ingredients, J. Agric. Food Chem. 58 (2010) 10518–10527, https://doi.org/10.1021/jf102391qG.E. Adamson, S.A. Lazarus, A.E. Mitchell, R.L. Prior, G. Cao, P.H. Jacobs, B. G. Kremers, J.F. Hammerstone, R.B. Rucker, K.A. Ritter, H.H. Schmitz, HPLC method for the quantification of procyanidins in cocoa and chocolate samples and correlation to total antioxidant capacity, J. Agric. Food Chem. 47 (1999) 4184–4188, https://doi.org/10.1021/jf990317m.S. Vertuani, E. Scalambra, T. Vittorio, A. Bino, A. Baldisserotto, S. Manfredini, Evaluation of antiradical activity of different cocoa and chocolate products: relation with lipid and protein composition, J. Med. Food 17 (2014) 512–516, https://doi.org/10.1089/jmf.2013.0110.V. Todorovic, I.R. Redovnikovic, Z. Todorovic, G. Jankovic, M. Dodevska, S. Sobajic, Polyphenols, methylxanthines, and antioxidant capacity of chocolate produced in Serbia, J. Food Compost Anal. 41 (2015) 137–143, https://doi.org/ 10.1016/j.jfca.2015.01.018S. Zapata-Bustamante, A. Tamayo-Tenorio, B. Alberto-Rojano, Efecto de la fermentacion ´ sobre la actividad antioxidante de diferentes clones de cacao colombiano, Rev. Cuba Plantas Med. 18 (2013) 391–404.L.J. Giraldo-Lopez, ´ Impact of fermentation and drying in polyphenol content and antioxidant capacity of cocoa variety CCN51, Rev. ION 29 (2016) 7–21, https:// doi.org/10.18273/revion.v29n2-2016001] D.B. Haytowitz, S.U.S.D.A. Bhagwat, Database for the Oxygen Radical Absorbance Capacity (ORAC) of Selected, Foods, Release 2 3 (2010) 10–48.A. Ricci, J.A. Arboleda, A. Versari, E. Chiarello, A. Bordoni, G.P. Parpinello, Microencapsulation of polyphenolic compounds recovered from red wine lees: process optimization and nutraceutical study, Food Bioprod. Process. 132 (2021) 1–12, https://doi.org/10.1016/j.fbp.2021.12.003F. Felice, A. Fabiano, M. De-Leo, A.M. Piras, D. Beconcini, M.M. Cesare, A. Braca, Y. Zambito, R. Di Stefano, Antioxidant effect of cocoa by-product and cherry polyphenol extracts: a comparative study, Antioxidants 9 (2020) 1–14, https://doi. org/10.3390/antiox9020132T.K. Kim, J.M. Hong, K.H. Kim, S.J. Han, I.C. Kim, H. Oh, J.H. Yim, Potential of ramalin and its derivatives for the treatment of alzheimer’s disease, Molecules 26 (2021) 1–12, https://doi.org/10.3390/molecules26216445.M.J. TallonAuthorised EU health claim for cocoa flavanols. Elsevier Ltd.,2015, ISBN 9781782423829..Z. Fang, B. Bhandari, Spray drying, freeze drying and related processes for food ingredient and nutraceutical encapsulation, ESI (2012) 73–109, https://doi.org/ 10.1533/9780857095909G. Ferreira, F. Matta, R. Augustus, D. Oliveira, Incorporation of spray dried and freeze dried blackberry particles in edible films: morphology, stability to pH, sterilization and biodegradation, Food Packag Shelf Life 20 (2019) 100313, https://doi.org/10.1016/j.fpsl.2019.100313.S. Krishnan, A.C. Kshirsagar, R.S. Singhal, The use of gum arabic and modified starch in the microencapsulation of a food flavoring agent, Carbohydr. Polym. 62 (2005) 309–315, https://doi.org/10.1016/j.carbpol.2005.03.020.R. Argüello-García, G.N. Quinonez-Bastidas, ˜ Catechins as emerging and promising antiparasitic agents, Biomed. J. Sci. Technol. Res. 30 (2020) 23065–23071, https://doi.org/10.26717/BJSTR.2020.30.004895.V. Bolanos, ˜ A. Díaz-Martínez, J. Soto, M.A. Rodríguez, C. Lopez-Camarillo, ´ L. A. Marchat, E. Ramírez-Moreno, The flavonoid (− )-epicatechin affects cytoskeleton proteins and functions in Entamoeba histolytica. J. Proteom. 111 (2014) 74–85, https://doi.org/10.1016/j.jprot.2014.05.017.M.B.G. Dos Reis, L.C. Manjolin, C.D.C. Maquiaveli, O.A. Santos-Filho, E.R. Da Silva, Inhibition of Leishmania (Leishmania) amazonensis and rat arginases by green tea EGCG,(+)-catechin and (− )-epicatechin: a comparative structural analysis of enzyme-inhibitor interactions, PLoS One 8 (2013) e78387, https://doi.org/ 10.1371/journal.pone.007J. Luo, H. Si, Z. Jia, D. Liu, Dietary anti-aging polyphenols and potential mechanisms, Antioxidants 10 (2021) 283, https://doi.org/10.3390/ antiox10020283.I. Bernatova, Biological activities of (− )-epicatechin and (− )-epicatechincontaining foods: Focus on cardiovascular and neuropsychological health, Biotechnol. Adv. 36 (2018) 666–681, https://doi.org/10.1016/j. biotechadv.2J. Oracz, E. Nebesny, D. Zyzelewicz, G. Budryn, B. Luzak, Bioavailability and metabolism of selected cocoa bioactive compounds: a comprehensive review, Crit. Rev. Food Sci. Nutr. 60 (2020) 1947–1985, https://doi.org/10.1080/ 10408398.2019.161916F.A. Tomas-Barberan, ´ E. Cienfuegos-Jovellanos, A. Marín, B. Muguerza, A. GilIzquierdo, B. Cerd´ a, J.C. Espín, A new process to develop a cocoa powder with higher flavonoid monomer content and enhanced bioavailability in healthy humans, J. Agric. Food Chem. 55 (2007) 3926–3935, https://doi.org/10.1021/ jf070121A.C. Aprotosoaie, A. Miron, A. Trifan, V.S. Luca, I.I. Costache, The cardiovascular effects of cocoa polyphenols -an overview, Diseases 4 (2016) 39, https://doi.org/ 10.3390/diseases40400H. Schroeter, C.L. Keen, H.D. Sesso, J.E. Manson, J.R. Lupton, Is this the end of (-)-epicatechin, or not? New study highlights the complex challenges associated with research into the cardiovascular health benefits of bioactive food constituents, Am. J. Clin. Nutr. 102 (2015) 975–976, https://doi.org/10.3945/ajcn.115.117283.E.A. Decker, Phenolics: prooxidants or antioxidants? Nutr. Rev. 55 (1997) 396–398, https://doi.org/10.1111/j.1753-4887.1997.tb01580.x.M. Hu, B. Wu, Z. Liu, Bioavailability of polyphenols and flavonoids in the era of precision medicine, Mol. Pharm. 14 (2017) 2861–2863, https://doi.org/10.1021/ acs.molpharmaceut.7b005© 2024 The Authorsinfo:eu-repo/semantics/openAccesshttp://purl.org/coar/access_right/c_abf2Atribución-NoComercial 4.0 Internacional (CC BY-NC 4.0)https://creativecommons.org/licenses/by-nc/4.0/AntioxidantChagas diseaseImmunomodulatorPolyphenolsTheobroma cacao LTrypanosoma cruziMicroencapsulation of Theobroma cacao L polyphenols: A high-value approach with in vitro anti-Trypanosoma cruzi, immunomodulatory and antioxidant activitiesArtículo de revistahttp://purl.org/coar/resource_type/c_2df8fbb1http://purl.org/coar/version/c_970fb48d4fbd8a85Textinfo:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionPublicationTEXTArtículo.pdf.txtArtículo.pdf.txtExtracted texttext/plain4242https://repositorio.unibague.edu.co/bitstreams/8ae7a3dc-cde2-4e7d-b45b-4b29aecf572d/download92a1fc35dbc11df82e6c692d26c672c9MD53THUMBNAILArtículo.pdf.jpgArtículo.pdf.jpgIM Thumbnailimage/jpeg28568https://repositorio.unibague.edu.co/bitstreams/d0b932fa-6283-4d11-ad3c-512938573ef2/download401bde7063cb29cf0a3b4cc23e963adfMD54LICENSElicense.txtlicense.txttext/plain; charset=utf-8134https://repositorio.unibague.edu.co/bitstreams/f63710c2-7e66-4b5b-b11f-229ba2614def/download2fa3e590786b9c0f3ceba1b9656b7ac3MD51ORIGINALArtículo.pdfArtículo.pdfapplication/pdf151017https://repositorio.unibague.edu.co/bitstreams/8e5e1242-e6f4-43c9-b1e7-ea47594dabe6/downloadfb7462534ecf918c68e610cb4a26426aMD5220.500.12313/5907oai:repositorio.unibague.edu.co:20.500.12313/59072025-11-07 03:02:43.163https://creativecommons.org/licenses/by-nc/4.0/© 2024 The Authorshttps://repositorio.unibague.edu.coRepositorio Institucional Universidad de Ibaguébdigital@metabiblioteca.comQ3JlYXRpdmUgQ29tbW9ucyBBdHRyaWJ1dGlvbi1Ob25Db21tZXJjaWFsLU5vRGVyaXZhdGl2ZXMgNC4wIEludGVybmF0aW9uYWwgTGljZW5zZQ0KaHR0cHM6Ly9jcmVhdGl2ZWNvbW1vbnMub3JnL2xpY2Vuc2VzL2J5LW5jLW5kLzQuMC8=

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