Potential of the flora of Peru emphasizing in the Asteraceae family against Trypanosoma cruzi

Guillermo E. Delgado-Paredes, Paulo R. Delgado Rojas, Consuelo Rojas Idrogo

Texto completo:

PDF (English)

Resumen

Introduction: American trypanosomiasis or Chagas diseases, caused by Trypanosoma cruzi and Human African trypanosomiasis, caused by Trypanosoma brucei, are two neglected tropical, endemic and fatal disease, that affect 20 million people and cause 95,000 deaths per year in tropical and subtropical areas of the world.

Objective: The objective of this review was to show the potential of the flora of Peru, emphasizing the Asteraceae family, against Trypanosoma cruzi, comparing it with American genera and species studied in various countries.

Methods: A review of scientific articles on the subject was carried out, especially taken from the Scopus, SciELO, ScienceDirect, Medline and PubMed databases of American plant species, covering a period of twelve years (2010 to 2022).

Results: A wide list of genera and species of the Asteraceae family and the flora of Peru with great potential in the treatment of trypanosomiasis is presented. Most of these species belong to the families Asteraceae, Piperaceae, Annonaceae, and Lauraceae. In the Asteraceae family, 48 genera and 76 species with trypanocidal activity were recorded, corresponding to 29 genera and 57 species for the flora of Peru. In these 29 genera, 174 endemic species potentially useful in the treatment of T. cruzi have been reported.

Conclusions: The flora of Peru has around 22,000 species. Some of these genera and species are found in the flora of various American countries and have been tested in the treatment of Chagas disease, so the flora of Peru offers new opportunities in its treatment.

Palabras clave

Chagas disease; crude extracts; medicinal plants; secondary metabolites; trypanosomiasis.

Referencias

Bermudez J, Davies C, Simonazzi A, Real JP, Palma S. Current drug therapy and pharmaceutical challenges for Chagas disease. Acta Trop. 2016;156:1-16. DOI: https://doi.org/10.1016/j.actatropica.2015.12.017

Villamizar LH, Cardoso MG, de Andrade J, Teixeira ML, Soares MJ. Linalool, a Piper aduncum essential oil component, has selective activity against Trypanosoma cruzi trypomastigote forms at 4 oC. Mem Inst Oswaldo Cruz. 2017;112:131-9. DOI: https://doi.org/10.1590/0074-02760160361

World Health Organization. Sustaining the Drive to Overcome the Global Impact of Neglected Tropical Diseases: Second WHO Report on Neglected Diseases. WHO. 2013 [access 01/04/2022]:138. Available from: https://apps.who.int/iris/handle/10665/77950

Molyneux DH, Asamoa-Bah A, Fenwick A, Savioli L, Hotez P. The history of the neglected tropical disease movement. Trans R Soc Trop Med Hyg. 2021;115:169-75. DOI: https://doi.org/10.1093/trstmh/trab015

Engels D, Xiao-Nong Z. Neglected tropical diseases: an effective global response to local poverty-related disease priorities. Infect Dis Poverty. 2020;9:10. DOI: https://doi.org/10.1186/s40249-020-0630-9

Frank FM, Ulloa J, Cazorla SI, Maravilla G, Malchiodi EL, Grau A, et al. Trypanocidal activity of Smallanthus sonchifolius: identification of active sesquiterpene lactones by bioassay-guided fractionation. Evid Based Complement Alternat Med. 2013:e627898. DOI: https://doi.org/10.1155/2013/627898

WHO-World Health Organization. Fact sheet Chagas disease (American tripanosomiasis). 2017 [access 01/04/2022]. Available from: http://www.who.int/mediacentre/factsheets/fs340/en/

Chan-Bacab MJ, Reyes-Estebanez MM, Camacho-Chab JC, Ortega-Morales BO. Microorganisms as a potential source of molecules to control trypanosomatid diseases. Molecules. 2021;26(5):1388. DOI: https://doi.org/10.3390/molecules26051388

Náquira C, Cabrera R. Breve Reseña Histórica de la Enfermedad de Chagas, a cien años de su Descubrimiento y Situación en el Perú. Rev Perú Med Exp Salud Pública. 2009;26(4):494-04.

Rojas J, Solís H, Palacios O. Evaluación in vitro de la actividad anti Trypanosoma cruzi de aceites esenciales de diez plantas medicinales. An Fac Med. 2010 [access 01/04/2022];71(3):161-5. Available from: http://www.scielo.org.pe/scielo.php?script=sci_arttext&pid=S1025-55832010000300004

González-Coloma A, Reina M, Sáenz C, Lacret R, Ruiz-Mesia L, Arán VJ, et al. Antileishmanial, antitrypanosomal, and cytotoxic screening of ethnopharmacologically selected Peruvian plants. Parasitol Res. 2012;110(4):1381-92. DOI: https://doi.org/10.1007/s00436-011-2638-3

Mejía-Parra JIJ, Pérez-Araujo MA, Roldán-Rodríguez J, Rojas-Idrogo C, Kato MJ, Delgado-Paredes GE. Actividad tripanocida de Piper solmsianum C. DC. sobre formas epimastigota y tripomastigota de Trypanosoma cruzi. Rev Cubana Med Trop. 2016 [access 01/04/2022];68(3):217-32. Available from: https://revmedtropical.sld.cu/index.php/medtropical/article/view/235

APG IV. The Angiosperm Phylogeny Group. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants. Bot J Linn Soc. 2016;181(1):1-20. Doi: https://doi.org/10.1111/boj.12385

Christenhusz MJM, Byng JW. The number of known plants species in the world and its annual increase. Phytotaxa 2016;261(3):201-17. DOI: https://doi.org/10.11646/phytotaxa.261.3.1

Brako L, Zarucchi JL. Catalogue of the Flowering Plants and Gymosperms of Peru. Monographs in Systematic Botany from the Missouri Botanical Garden. 1993;45:1286. ISBN: 09-152-79193.

Ulloa C, Zarucchi JL, León B. Diez años de adiciones a la flora del Perú: 1993-2003. Arnaldoa (Edic. Especial):Trujillo, Perú; 2004. 1-242 pp.

Astelbauer F, Walochnik J. Antiprotozoal compounds: state of the art and new developments. Int J Antimicrob Agents 2011;38:118-124. DOI: https://doi.org/10.1016/j.ijantimicag.2011.03.004

Alviano DS, Barreto ALS, Dias FA, Rodrigues IA, Rosa MSS, Alviano CS, et al. Conventional therapy and promising plant-derived compounds against trypanosomatid parasites. Front Microbiol. 2012;3:1-10:a283. DOI: https://doi.org/10.3389/fmicb.2012.00283

Clemons KV, Sobel RA, Martínez M, Correa-Oliveira R, Stevens DA. Lack of efficacy of liposomal amphotericin B against acute and chronic Trypanosoma cruzi infection in mice. Am J Trop Med Hyg. 2017;97:1141-6. DOI: https://doi.org/10.4269/ajtmh.16-0975

López-Arencibia A, San Nicolás-Hernández D, Bethencourt-Estrella CJ, Sifaoui I, Reyes-Batlle M, Rodríguez-Expósito RL, et al. Withanolides from Withania aristata as antikinetoplastid agents through induction of programmed cell death. Pathogens. 2019;1;8(4):172. DOI: https://doi.org/10.3390/pathogens8040172

Sales Junior PA, Molina I, Fonseca Murta SM, Sánchez-Montalvá A, Salvador F, Corrêa-Oliveira R, et al. Experimental and clinical treatment of Chagas Disease. Am J Trop Med Hyg. 2017;97:1289-03. DOI: https://doi.org/10.4269/ajtmh.16-0761

Kawaguchi WH, Cerqueira LB, Fachi MM, Campos ML, Reason IJM, Pontarolo R. Efficacy and safety of Chagas disease drug therapy and treatment perspectives. In: V. Nissapatorn and HS Oz, eds. Chagas Disease-Basic Investigations and Challenges. IntechOpen. 2018;1:121-51. DOI: https://doi.org/10.5772/Intechopen.74845

Dickie AE, Giordanji F, Gould MK, Mäser P, Burri C, Mottram JC, et al. New drugs for human African trypanosomiasis: A twenty first century success story. Trop Med Infect Dis. 2020;5(1):29. DOI: https://doi.org/10.3390/tricalmed5010029

De Koning HP. The drugs of sleeping sickness: Their mechanisms of action and resistance, and a brief history. Trop Med Infec Dis. 2020;5(1):14. DOI: https://doi.org/10.3390/tricalmed5010014

Atanasov AG, Waltenberger B, Pferschy-Wenzig EM, Linder T, Wawrosch C, Uhrin P, et al. Discovery and resupply of pharmacologically active plant-derived natural products: a review. Biotechnol Adv. 2015;33:1582-14. DOI: https://doi.org/10.1016/j.biotechadv.2015.08.001

Pereira RM, Creco GMZ, Moreira AM, Chagas PF. Applicability of plant-based products in the treatment of Trypanosoma cruzi and Trypanosoma brucei infections: a systematic review of periclinal in vivo evidence. Parasitology 2017;144:1275-87. DOI: https://doi.org/10.1017/S0031182017000634

Corrêa DS, Tempone AG, Reimão JQ, Taniwaki NN, Romoff P, Fávero OA, et al. Anti-leishmanial and anti-trypanosomal potential of polygodial isolated from stem barks of Drimys brasiliensis Miers (Winteraceae). Parasitol Res. 2011;109:231-6. DOI: https://doi.org/10.1007/s00436-010-2229-8

Pelizzaro-Rocha KJ, Veiga-Santos P, Lazarin-Bidóia D, Ueda-Nakamura T, Dias Filho BP, Ximenes VF, et al. Trypanocidal action of eupomatenoid-5 is related to mitocondrial dysfunction and oxidative damage in Trypanososma cruzi. Microbes Infect. 2011;13:1018-24. DOI: https://doi.org/10.1016/j.micinf.2011.05.011

de Oliveira A, Mesquita JT, Tempone AG, Lago JH, Guimaraes EF, Kato MJ. Leishmanicidal activity of an alkenylphenol from Piper malacophyllum is related to plasma membrane disruption. Exp Parasitol. 2012;132:383-7. DOI: https://doi.org/10.1016/j.exppara.2012.08.019

Esperandim VR, Ferreira DS, Rezende KCS, Cunha WR, Saraiva J, Bastos JK, et al. Evaluation of the in vivo therapeutic properties of (-)-cubebin and (-)-hinokinin against Trypanosoma cruzi. Exp Parasitol. 2013;133(4):442-6. DOI: https://doi.org/10.1016/j.exppara.2012.12.005

García-Huertas P, Olmo F, Sánchez-Moreno M, Domínguez J, Chahboun R, Triana-Chávez O. Activity in vitro and in vivo against Trypanosoma cruzi of a furofuran lignan isolated from Piper jericoense. Exp Parasitol. 2018;189:34-42. DOI: https://doi.org/10.10167j.exppara.2018.04.009

Sartorelli P, Carvalho CS, Reimão JQ, Lorenzi H, Tempone AG. Antritrypanosomal activity of a diterpene and lignans isolated from Aristolochia cymbifera. Planta Med. 2010;76(13):1454-56. DOI: https://doi.org/10.1055/s-0029-1240952

Oliani J, Siqueira CAT, Sartoratto A, Queiroga CL, Moreno PRH, Reimão JQR, et al, Chemical composition and in vitro antiprotozoal activity of the volatile oil from laeves of Annona crassifolia Mart. (Annonaceae). Pharmacol OnLine. 2013;3:8-15. DOI: http://doi.org/pharmacologyonline.silae.it

Siqueira CAT, Oliani J, Sartoratto A, Queiroga CL, Moreno PRH, Reimao JQ, et al. Chemical constituents of the volatile oil from leaves of Annona coriacea and in vitro antiprotozoal activity. Rev Bras Farmacogn. 2011;21(1):33-40. DOI: https://doi.org/10.1590/S0102-695X2011005000004

Cabral MMO, Barbosa-Filho JM, Maia GLA, Chaves MCO, Braga MV, De Souza W, et al. Neolignans from plants in northeastern Brazil (Lauraceae) with activity against Trypanosoma cruzi. Exp Parasitol. 2010;124:319-4. DOI: https://doi.org/10.1016/j.exppara.2009.11.007

Morais TR, Conserva GAA, Varela MT, Costa-Silva TA, Thevenard F, Ponci V, et al. Improving the drug-likeness of inspiring natural products – evaluation of the antiparasitic activity against Trypanososma cruzi through semi-synthetic and simplified analogues of licarin A. Sci Rep. 2020;10(1):5467. DOI: https://doi.org/10.1038/s41598-020-62352-w

Conserva GA, Quiros-Guerrero LM, Costa-Silva TA, Marcourt L, Pinto EG, Tempone AG, et al. Metabolite profile of Nectandra oppositifolia Nees & Mart. and assessment of antitrypanosomal activity of bioactive compounds through efficiency analysis. PLoS One. 2021;16:e0247734. DOI: https://doi.org/10.1371/journal.pone.0247334

Conserva GA, Costa-Silva TA, Quirós-Guerrero LM, Marcourt L, Wolfender J-L, Queiroz EF, et al. Kaempferol-3-O—(3,4-di-E-p-coumaroyl)-rhamnopyranoside from Nectandra oppositifolia releases Ca2+ from intracellular pools of Trypanosoma cruzi affecting the bioenergetics system. Chem Biol Interac. 2021;3491:e109661. DOI: https://doi.org/10.1016/j.cb1.2021.109661

Grecco SS, Costa-Silva TA, Jerz G, de Sousa FS, Londero VS, Galuppo MK, et al. Neolignans from leaves of Nectandra leucantha (Lauraceae) display in vitro antitrypanosomal activity via plasma membrane and mitocondrial damages. Chem Biol Interact. 2017;277:55-61. DOI: https://doi.org/10.1016/j.cbi.2017.08.017

Grecco SS, Letsyo E, Tempone AG, Lago JHG, Jerz G. Electrospray mass-spectrometry guided target isolation of neolignans from Nectandra leucantha (Lauraceae) by high performance- and spiral-coil countercurrent chromatography. J Chromatogr A. 2019;1608:460422. DOI: https://doi.org/10.1016/j.chroma.2019.460422

Ponci V, Figueiredo CR, Massaoka MH, de Farias CF, Matsuo AL, Sartorelli P, et al. Neolignans from Nectandra megapotamica (Lauraceae) display in vitro cytotoxic activity end induce apoptosis in leukemia cells. Molecules. 2015;20:12757-68. DOI: https://doi.org/10.3390/molecules200712757

da Silva YC, Silva EMS, Fernandes NdeS, Lopes NL, Orlandi PP, Nakamura CV, et al. Antimicrobial substances from Amazonian Aniba (Lauraceae) species. Nat Prod Res. 2021a;35:849-52. DOI: https://doi.org/10.1080/14786419.2019.1603225

Rodríguez-Hernández KD, Martínez I, Agredano-Moreno LT, Jiménez-García LF, Reyes-Chilpa R, Espinoza B. Coumarins isolated from Calophyllum brasiliense produce ultrastructural alterations and affect in vitro infectivity of Trypanosoma cruzi. Phytomedicine. 2019;61:152827. DOI: https://doi.org/10.1016/j.phytomed.2019.152827

Rodríguez-Hernández KD, Martínez I, Reyes-Chilpa R, Espinoza B. Mammea type coumarins isolated from Calophyllum brasiliense induced apoptotic cell death of Trypanosoma cruzi through mitocondrial dysfunction, ROS production and cell cycle alterations. Bioorg Chem. 2020;100:103894. DOI: https://doi.org/10.1016/j.bioorg.2020.103894

Reyes-Chilpa R, Estrada-Muñiz E, Veja-Avila E, Abe F, Kinjo J, Hérnandez-Ortega S. Trypanocidal constituents in plants Mammea-type coumarins. Mem Inst Oswaldo Cruz. 2008;103:431-6. DOI: https://doi.org/10.1590/s0074-02762008000500004

Bou DD, Tempone AG, Pinto ÉG, Lago JH, Sartorelli P. Antiparasitic activity and effect of casearins isolated from Casearia sylvestris on Leishmania and Trypanosoma cruzi plasma membrane. Phytomedicine. 2014;21(5):676-81. DOI: https://doi.org/10.1016/j.phytomed.2014.01.004

dos Santos AL, Amaral M, Hasegawa FR, Lago JHG, Tempone AG, Sartorelli P. (-)-T-Cadinol a sesquiterpene isolated from Casearia sylvestris (Salicaceae) displayed in vitro activity and causes hyperpolarization of the membrane potential of Trypanosoma cruzi. Front Pharmacol. 2022;13:e865432. DOI: https://doi.org/10.3389/fphar.2021.734127

Fernandes PAS, da Silva JCP, Lima Sales D, Ribeiro PRV, Sousa de Brito E, Kerntopf MR, et al. Chemical constituents and biological activities of Croton heliotropiifolius Kunth. Antibiotics. 2021;10:e1074. DOI: https://doi.org/10.3390/antibiotics10091074

Cordeiro TDM, Borghetti F, Oliveira SCC, Bastos IMD, de Santana JM, Grellier P, et al. Brazilian Cerrado Qualea grandiflora Mart. leaves exhibit antiplasmodial and tripanocidal activities in vitro. Pharmacogn Mag. 2017;13(52):668-2. DOI: https://doi.org/10.4103/pm.pm_100_17

Santos KKA, Matias EFF, Tintino SR, Souza CES, Braga MFBM, Guedes GMM, et al. Anti-Trypanosoma cruzi and cytotoxic activities of Eugenia uniflora. Exp Parasitol. 2012;131:130-2. DOI: https://doi.org/10.1016/j.exppara.2012.02.019

Correa E, Quiñones W, Robledo S, Carrillo L, Archbold R, Torres F, et al. Leishmanicidal and trypanocidal activity of Sapindus saponaria. BLACPMA. 2014 [access 01/04/2022];13(4):311-23. Available from: https://www.redalyc.org/articulo.oa?id=85631435001

Ferreira ME, Cebrián-Torrejón G, Corrales AS, Bilbao NV, Rolón M, Gómez CV, et al. Zanthoxylum chiloperone leaves extract: first sustainable Chagas disease treatment. J Ethnopharmacol. 2011;133:986-93. DOI: https://doi.org/10.1016/j.jep.2010.11.032

Araújo CRR, Silva RR, Silva TM, Takahashi JA, Sales-Junior PA, Dessimonio-Pinto NAV, et al. Constituents from stem barks of Luehea ochrophylla Mart and evaluation of their antiparasitic, antimicrobial, and antioxidant activities. Nat Prod Res. 2017;31(16):1948-53. DOI: https://doi.org/10.1080/14786419.2016.1266346

Pertino MW, Vega C, Rolón M, Coronel C, Rojas A, Schmeda-Hirschmann G. Antiprotozoal activity of triazole derivatives of dehydroabietic acid and olenolic acid. Molecules. 2017;22(3):e369. DOI: https://doi.org/10.3390/molecules22030369

Escobar P, Leal SM, Herrera LV, Martínez JR, Stashenko E. Chemical composition and antiprotozoal activities of Colombian Lippia spp. essential oils and their major components. Mem Inst Oswaldo Cruz. 2010;105:184-90. DOI: https://doi.org/10.1590/S0074-02762010000200013

Borges AR, Aires JRDA, Higino TMM, de Medeiros MDGF, Citó AMDGL, Lopes JAD, et al. Trypanocidal and cytotoxic activities of essential oils from medicinal plants of Northeast of Brazil. Exp Parasitol. 2012;132:123-8. DOI: https://doi.org/10.1016/j.exppara.2012.06.003

de Melo ARB, Maciel Higino TM, da Rocha Oliveira ADP, Fontes A, da Silva DCN, de Castro MCAB, et al. Lippia sidoides and Lippia origanoides essential oils affect the viability, motility and ultrastructure of Trypanosoma cruzi. Micron. 2020;129:102781. DOI: https://doi.org/10.1016/j.micron.2019.102781

Oliveira CVB, da Silva PAG, Tintino SR, Coronel CC, Gómez MCV, Rolón M, et al. A potential new source of therapeutic agents for the treatment of mucocutaneous leishmaniasis: the essential oil of Rhaphiodon echinus. Molecules. 2022;27:e2169. DOI: https://doi.org/10.3390/molecules27072169

Althaus JB, Kaiser M, Brun R, Schmidt TJ. Antiprotozoal activity of Achillea ptarmica (Asteraceae) and its main alkamide constituents. Molecules. 2014;19:6428-38. DOI: https://doi.org/10.3390/molecules19056428

Moraes-Neto RN, Setúbal RFB, Higino TMM, Brelaz-de-Castro MCA, da Silva LCN, dos Santos Aliança AS. Asteraceae plants as sources of compounds against leishmaniasis and Chagas diseases. Front Pharmacol. 2019;10:477. DOI: https://doi.org/10.3389/fphar.2019.00477

Beer MF, Frank FM, Elso OG, Bivona AE, Cerny N, Giberti G, et al. Trypanocidal and leishmanicidal activities of flavonoids isolated from Stevia satureiifolia var. satureiifolia. Pharm Biol. 2016;54(10):2188-95. DOI: https://doi.org/10.3109/13880209.2016.1150304

Elso OG, Bivona AE, Alberti AS, Cerny N, Fabian L, Morales C, et al. Trypanocidal activity of four sesquiterpene lactones isolated from Asteraceae species. Molecules. 2020;25:e2014. DOI: https://doi.org/10.3390/molecules25092014

Elso OG, Puente V, Barrera P, Sosa-Escudero MA, Sülsen VP, Lombardo ME. Mode of action of the sesquiterpene lactones eupatoriopicrin and estafetin on Trypanosoma cruzi. Phymomedicine. 2022;96:e153900. DOI: https://doi.org/10.1016/j.phymed.20231.153900

Sülsen VP, Lizarraga EF, Elso OG, Cerny N, Alberti AS, Bivona AE, et al. Activity of estafietin and analogues on Trypanosoma cruzi and Leishmania braziliensis. Molecules. 2019;24:e1209. DOI: https://doi.org/10.3390/molecules24071209

Gonçalves MD, Bartoleti BTS, Tomiotto-Pellissier F, Concato VM, de Matos RLN, Silva TF, et al. 2022. Grandiflorenic acid isolated from Sphagneticola trilobata against Trypanosoma cruzi: toxicity, mechanisms of action and immunomodulation. Toxicol in Vitro. 2022;78:e105267. DOI: https://doi.org/10.1016/j.tiv.2021.105267

Da Silva CF, Batista DDAG, De Araújo JS, Batista MM, Lionel J, De Souza EM, et al. Activities of psilostachyin A and cynaropicrin against Trypanosoma cruzi in vitro and in vivo. Antimicrob Agents Chemother. 2013;57(11):5307-14. DOI: https://doi.org/10.1128/AAC.00595-13

Adessi TG, Ana Y, Stempin CC, García MC, Bisogno FR, Nicotra VE, García ME, et al. Psilostachyins trypanocidal compounds: bioguided fractionation of Ambrosia tenuifolia chemically modified extract. Phytochemistry. 2022;194:e113014. DOI: https://doi.org/10.1016/j.phytochem.2021.113014

Beer MF, Reta GF, Puerta A, Bivona AE, Alberti AS, Cerny N, et al. Oxonitrogenated derivatives of eremophilans and eudesmans: Antiproliferative and Anti-Trypanosoma cruzi Activity. Molecules. 2022;27:3067. DOI: https://doi.org/10.3390/molecules27103067

Sudan CRC, Pereira LC, Silva AF, Moreira CPDES, De Oliveira DS, Faria G, et al. Biological activities of extracts from Ageratum fastigiatum: phytochemical study and in silico target fishing approach. Plant Med. 2021;87:1045-61. DOI: https://doi.org/10.1055/a-1576-4080

Sepúlveda-Robles O, Espinoza-Gutiérrez B, Gómez-Verjan JC, Guzmán-Gutiérrez SL, De Ita M, Silva-Miranda M, et al. Trypanocidal and toxicological assessment in vitro and in silico of three sesquiterpene lactones from Asteraceae plant species. Food Chem Toxicol. 2019;125:55-61. DOI: https://doi.org/10.1016/j.fct.2018.12.023

Grecco SS, Reimão JQ, Tempone AG, Sartorelli P, Cunha RL, Romoff P, et al. In vitro antileishmanial and antitrypanosomal activities of flavanones from Baccharis retusa DC. (Asteraceae). Exp Parasitol. 2012;130(2):141-5. DOI: https://doi.org/10.1016/j.exppara.2011.11.002

Grecco SS, Reimão JQ, Tempone AG, Sartorelli P, Romoff P, Ferreira MJ, et al. Isolation of an antileishmanial and antitrypanosomal flavonone from the leaves of Baccharis retusa DC. (Asteraceae). Parasitol Res. 2010,106(5):1245-8. DOI: https://doi.org/10.1007/s00436-010-1771-8

Ueno AK, Barcellos AF, Costa-Silva TA, Mesquita JT, Ferreira DD, Tempone AG, et al. Antitrypanosomal activity and evaluation of the mechanism of action of diterpenes from aerial parts of Baccharis retusa (Asteraceae). Fitoperapia. 2018;125:55-8. DOI: https://doi.org/10.1016/j.fitote.2017.12.016

Grecco SS, Félix MJ, Lago JH, Pinto EG, Tempone AG, Romoff P, et al. Anti-trypanosomal phenolic derivatives from Baccharis uncinella. Nat Prod Commun. 2014;9:171-3. DOI: https://doi.org/10.1177/1934578X1400900210

Ferretti MD, Rodriguez MV, Ferretti A, Nocito I, Bettucci GR, Srebot MS, et al. Antiprotozoal effect of Baccharis spicata and B. punctata volatile oils and their active components against Trypanosoma cruzi. Rev Bras Farmacogn. 2022;32:133-8. DOI: https://doi.org/10.1007/s43450-021-00226-6

da Costa-Silva TA, Silva ML, Antar GM, Tempone AG, Lago JHG. Ent-kaurane diterpenes isolated from n-hexane extract of Baccharis sphenophylla by bioactivity-guided fraction target the acidocalcisomes in Trypanosoma cruzi. Phytomedicine. 2021;93:153748. DOI: https://doi.org/10.1016/j.phymed.2021.153748

Silva ML, Costa-Silva TA, Antar GM, Tempone AG, Lago JHG. Chemical constituents from aerial parts of Baccharis sphenophylla and effects against intracellular forms of Trypanosoma cruzi. Chem Biodivers. 2021;18(10):e2100466. DOI: https://doi.org/10.1002/cbdv.202100466

Pelizzaro-Rocha KJ, Tiuman TS, Izumi E, Ueda-Nakamura T, Dias Filho BP, Nakamura CV. Synergistic effects of parthenolide and benznidazole on Trypanosoma cruzi. Phytomedicine. 2010;18(1):36-9. DOI: https://doi.org/10.1016/j.phymed.2010.09.005

Cogo J, Caleare Ade O, Ueda-Nakamura T, Filho BP, Ferreira IC, Nakamura CV. Trypanocidal activity of guaianolide obtained from Tanacetum parthenium (L.) Schultz-Bip. and its combinational effect with benznidazole. Phytomedicine. 2012;20(1):59-66. DOI: https://doi.org/10.1016/j.phymed.2012.09.011

Quintero-Pertuz H, Veas-Albornoz R, Carrillo I, González-Herrera F, Lapier M, Carbonó-Delahoz, et al. 2022. Trypanocidal effect of alcoholic extract of Castanedia santamartensis (Asteraceae) leaves is based on altered mitochondrial function. Biomed Pharmacother. 2022;148:e112761. DOI: https://doi.org/10.1016/j.biopha.2022.112761

Pereira CG, Moraes CB, Franco CH, Feltrin C, Grougnet R, Barbosa EG, et al. In vitro anti-Trypanosoma cruzi activity of halophytes from southern Portugal reloaded: A especial focus on sea fennel (Crithmum maritmum L.). Plants. 2021;10:e2235. DOI: https://doi.org/10.3390/plants10112235

Lima TC, Souza RJ, Santos AD, Moraes MH, Biondo NE, Barison A, et al. Evaluation of leishmanicidal and trypanocidal activities of phenolic compounds from Calea uniflora Less. Nat Prod Res. 2016;30(5):551-7. DOI: https://doi.org/10.1080/14786419.2015.1030740

Lima TC, Souza RJ, Moraes MH, Matos SS, Almeida FHO, Steindel M, et al. Isolation and characterization of sesquiterpene lactones from Calea uniflora Less. annd their leishmanicidal and trypanocidal activities. Quím Nova. 2021;44:696-9. DOI: https://doi.org/10.21577/0100-4042.20170728

Lima TC, Souza RDJ, Moraes MH, Steindel M, Biavatti MW. A new furanoheliangolide sesquiterpene lactone from Calea pinnatifolia (R. Br.) Less (Asteraceae) and evaluation of its trypanocidal and leishmanicidal activities. J Braz Chem Soc. 2017;28(2):367-75. DOI: https://doi.org/10.5935/0103-5053.20160186

Elso OG, Clavin M, Hernández N, Sgarlata T, Bach H, Catalan CAN, et al. Antiprotozoal compounds from Urolepis hecatantha (Asteraceae). Evid Based Complement Alternat Med. 2021:e6622894. DOI: https://doi.org/10.1155/2021/6622894

Lucarini R, Magalhaes LG, Rodrigues V, Souza JM, Tozatti MG, Pires RH, et al. Antiprotozoal and antihelmintic evaluation of the hydroalcoholic extract, fractions and compounds of Gochnatia pulchra. Lat Am J Pharm. 2016; [access 01/04/2022];35(4):762-67. Available from: http://www.latamjpharm.org/resumenes/35/4/LAJOP_35_4_1_17.pdf

Machado VR, Sandjo LP, Pinheiro GL, Moraes MH, Steindel M, Pizzolatti MG, et al. Synthesis of lupeol derivatives and their antileishmanial and antitrypanosomal activities. Nat Prod Res. 2018;32(3):275-81. DOI: https://doi.org/10.1080/14786419.2017.1353982

Martins MM, De Aquino FJT, De Oliveira A, Do Nascimiento EA, Chang R, Borges MS, et al. Chemical composition, antimicrobial and antiprotozoal activity of essential oils from Vernonia brasiliana (Less) Druce (Asteraceae). J Essent Oil-Bear Plants. 2015;18(3):561-9. DOI: https://doi.org/10.1080/0972060X.2014.895683

Sosa A, Salamanca Capusiri E, Amaya S, Bardón A, Giménez-Turba A, et al. Trypanocidal activity of South American Vernoniae (Asteraceae) extracts and its sesquiterpene lactones. Nat Prod Res. 2021;35:5224-8. DOI: https://doi.org/10.1080/14786419.2020.1739682

Morais TR, Romoff P, Fávero OA, Reimão JQ, Lourenço WC, Tempone AG, et al. Anti-malarial, anti-trypanosmal, and antileishmanial activities of jacaranone isolated from Pentacalia desiderabilis (Vell.) Cuatrec. (Asteraceae). Parasitol Res. 2012;110(1):95-101. DOI: https://doi.org/10.1007/s00436-011-2454-9

Nogueira MS, Da Costa FB, Brun R, Kaiser M, Schmidt TJ. Ent-pimarane and ent-kaurane diterpenes from Aldama discolor (Asteraceae) and their antiprotozoal activity. Molecules. 2016;21(9):e1237. DOI: https://doi.org/10.3390/molecules21091237

Larrazábal-Fuentes MJ, Fernández-Galleguillos C, Palma-Ramírez J, Romero-Parra J, Sepúlveda K, Galetovic A, et al. Chemical profiling, antioxidant, anticholinesterase, and antiprotozoal potentials of Artemia copa Phil. (Asteraceae). Front Pharmacol. 2020;11:e594174. DOI: https://doi.org/10.3389/fphar.2020.594174

Zeouk I, Sifaoui I, López-Arencibia A, Reyes-Batlle M, Bethencourt-Estrella CJ, Bazzocchi IL, et al. Sesquiterpenoids and flavonoids from Inula viscosa induce programmed cell death in kinetoplastids. Biomed Pharmacother. 2020;130:e110518. DOI: https://doi.org/10.1016/j.biopha.2020.110518

Laurella LC, Frank FM, Sarquiz A, Alonso MR, Giberti G, Cavallaro L, et al. In vitro evaluation of antiprotozoal and antiviral activities of extracts from Argentinean Mikania species. Sci World J. 2012:121253. DOI: https://doi.org/10.1100/2012/121253

Laurella LC, Cerny N, Bivona AE, Sánchez Alberti A, Giberti G, Malchiodi EL, et al. Assessment of sesquiterpene lactones isolated from Mikania plants species for their potential efficacy against Trypanosoma cruzi and Leishmania sp. PLoS Negl Trop Dis. 2017;11(9):e0005929. DOI: https://doi.org/10.1371/journal.pntd.0005929

Puente V, Laurella LC, Spina RM, Lozano E, Martino VS, Sosa MA, et al. Primary targets of the sesquiterpene lactone deoxymikanolide on Trypanosoma cruzi. Phytomedicine. 2019;56:27-4. DOI: https://doi.org/10.1016/j.phytomed.2018.10.015

Galkina A, Krause N, Lenz M, Daniliuc CG, Kaiser M, Schmidt TJ. Antitrypanosomal activity of sesquiterpene lactones from Helianthus tuberosus L. including a new furanoheliangolide with an unusual structure. Molecules. 2019;24:e1068. DOI: https://doi.org/10.3390/molecules24061068

Sülsen V, Barrera P, Muschietti L, Martino V, Sosa M. Antiproliferative effect and ultrastructural alterations induced by psilostachyin on Trypanosoma cruzi. Molecules. 2010;15(1):545-53. DOI: https://doi.org/10.3390/molecules15010545

Sülsen VP, Frank FM, Cazorla SI, Barrera P, Freixa B, Vila R, et al. Psilostachyin C: a natural compound with trypanocidal activity. Int J Antimicrob Agents. 2011;37(6):536-43. DOI: https://doi.org/10.1016/j.ijantimicag.2011.02.003

Sülsen VP, Cazorla SI, Frank FM, Laurella LC, Muschietti LV, Catalán CA, et al. Natural terpenoids from Ambrosia species are active in vitro and in vivo against human pathogenic trypanosmatids. PLoS Negl Trop Dis. 2013;7(10):e2494. DOI: https://doi.org/10.1371/journal.pntd.0002494

Sülsen VP, Puente V, Papademetrio D, Batlle A, Martino VS, Frank FM, et al. Mode of action of the sesquiterpene lactones psilostatachin and psilostachyin C on Trypanosoma cruzi. PLoS ONE. 2016;11(3):e0150526. DOI: https://doi.org/10.1371/journal.pone.0150526

Ulloa JL, Spina R, Casasco A, Petray PB, Martino V, Sosa MA, et al. Germacranolide-type sesquiterpene lactones from Smallanthus sonchifolius with promising activity against Leishmania mexicana and Trypanosoma cruzi. Parasit Vectors. 2017;10(1):567. DOI: https://doi.org/10.1186/s13071-017-2509-6

Sales Junior PA, Zani CL, de Siquiera EP, Kohlhoff M, Marques FR, Caldeira ASP, et al. Trypanocidal trixikingolides from Trixis vauthieri. Nat Prod Res. 2021;35:2691-99. DOI: https://doi.org/10.1080/14786419.2019.1663510

Varela J, Lavaggi ML, Cabrera M, Rodríguez A, Miño P, Chiriboga X, et al. Bioactive-guided identification of labdane diterpenoids from aerial parts of Aristeguietia glutinosa as anti-Trypanosoma cruzi agents. Nat Prod Commun. 2012;7(9):1139-42. DOI: https://doi.org/10.1177/1934578X1200700907

Varela J, Serna E, Torres S, Yaluff G, de Bilbao NI, Miño P, et al. In vivo anti-Trypanososma cruzi activity of hydro-ethanolic extract and isolated active principles from Aristeguietia glutinosa and mechanism of action studies. Molecules. 2014;19(6):8488-02. DOI: https://doi.org/10.3390/molecules190 68488

Gutiérrez YI, Scull R, Villa A, Satyal P, Cos P, Monzote L, et al. Chemical composition, antimicrobial and antiparasitic screening of the essential oil from Phania matricarioides (Spreng.) Griseb. Molecules. 2019;24:e1615. DOI: https://doi.org/10.3390/molecules24081615

Bailen M, Martínez-Díaz RA, Hoffmann JJ, González-Coloma A. Molecular diversity from arid-land plants: valorization of terpenes and biotransformation products. Chem Biodivers. 2020;17:e1900663. DOI: https://doi.org/10.1002/cbdv.201900663

Selener MG, Elso OG, Grosso C, Borgo J, Clavin M, Malchiodi EL, et al. Anti-Trypanosoma cruzi activity of extracts from Argentineae Asteraceae species. Iran J Pharm Res. 2019;18:1854-61. DOI: https://doi.org/10.22037/ijpr.2019.14491.12430

Calderón AI, Romero LI, Ortega-Barría E, Solís PN, Zacchino S, Giménez A, et al. Screening of Latin American plants for antiparasitic activities against malaria, Chagas disease, and leishmaniasis. Pharm Biol. 2010;48:545-53. DOI: https://doi.org/10.3109/13880200903193344

Castillo UG, Komatsu A, Martínez ML, Menjívar J, Núñez MJ, Uekusa Y, et al. Anti-trypanosomal screening of Salvadoran flora. J Nat Med. 2022;76:259-67. DOI: https://doi.org/10.1007/s11418-021-01562-6

Peres RB, Fiuza LFDA, da Silva PB, Batista MM, Camillo FDAC, Marques AM, et al. In vitro phenotypic activity and in silico analysis of natural products from Brazilian biodiversity on Trypanosoma cruzi. Molecules. 2021;26:e5676. DOI: https://doi.org/10.3390/molecules26185676

Charneau S, de Mesquita ML, Bastos IM, Santana JM, de Paula JE, Grellier P, et al. In vitro investigation of Brazilian Cerrado plant extract activity against Plasmodium falciparum, Trypanosoma cruzi and T. brucei gambiense. Nat Prod Res. 2016;30(11):1320-6. DOI: https://doi.org/10.1080/14786419.2015.1055264

Castañeda JS, Suta-Velásquez M, Mateus J, Pardo-Rodríguez D, Puerta Concepción J. Cuéllar A, et al. Preliminary chemical characterization of ethanolic extracts from Colombian plants with promising anti-Trypanosoma cruzi activity. Exp Parasitol. 2021;223:e108079. https://doi.org/10.1016/j.exppara.2021.108079

Teixeira TL, Teixeira SC, Da Silva CV, De Souza MA. Potential therapeutic use of herbal extracts in trypanosomiasis. Pathog Glob Health. 2014;108(1):30-6. DOI: https://doi.org/10.1179/2047773213Y.0000000120

Muñoz OM, Mayab JD, Ferreira J, Christen P, San Martin J, López-Muñoz R, et al. 2013. Medicinal plants of Chile: Evaluation of their Anti-Trypanosoma cruzi activity. Z. Naturforsch. 2013;68:198-2. DOI: https://doi.org/10.1515/znc-2013-5-605

Pérez KC, Galaviz L, Iracheta JM, Lucero EA, Molina ZJ. Actividad contra Trypanosoma cruzi (Kinetoplastida: Trypanosomatidae) de extractos metanólicos de plantas de uso medicinal en México. Rev Biol Trop. (Int J Trop Biol) 2017;65:1459-69. DOI: https://doi.org/10.15517/rbt.v65i4.27153

Oliveira de Souza LI, Bezzera-Silva PC, Navarro DMAF, da Silva AG, Correia MTS, da Silva MV, et al. The chemical composition and trypanocidal activity of volatile oils from Brazilian Caatinga plants. Biomed Pharmacother. 2017;96:1055-64. DOI: https://doi.org/10.1016/j.biopha.2017.11.121

Biodiversidad en el Perú. 2019 [access 01/04/2022]. Available from: https://www.lima2019.pe/biodiversidad-en-el-peru

Bussmann RW, Glenn A. Medicinal plants used in Peru for the treatment of respiratory disorders. Rev Peruana Biol. 2010;17:331-46. Versión Online ISSN 1727-9933.

Vásquez L, Escurra J, Aguirre R, Vásquez G, Vásquez P. Plantas Medicinales en el Norte del Perú. FINCyT: Lambayeque – Perú. 2010;382 p.

Delgado-Paredes GE, Delgado-Rojas PR, Rojas-Idrogo C. Peruvian plants of traditional use as potential sources of molecules with activity against COVID-19. Rev Cubana Med Trop. 2021 [access 01/04/2022];73(3):e671. Available from: https://revmedtropical.sld.cu/index.php/medtropical/article/view/671/539

Goyzueta-Mamani LD, Barazorda-Ccahuana HL, Mena-Ulecia K, Chávez-Fumagalli MA. Antiviral activity of metabolites from Peruvian plants against SARS-CoV-2: An in silico approach. Molecules. 2021;26:3882. DOI: https://doi.org/10.3390/molecules26133882

Villena-Tejada M, Vera-Ferchau I, Cardona-Rivero A, Zamalloa-Cornejo R, Quispe-Flórez M, Frisancho-Triveño Z, et al. Use of medicinal plants for COVID-19 prevention and respiratory symptom treatment during the pandemic in Cusco, Peru: A cross-sectional survey. PLoS ONE. 2021;16(9):e0257165. DOI: https://doi.org/10.1371/journal.pone.0257165

Enlaces refback

  • No hay ningún enlace refback.




Copyright (c) 2024 Guillermo Eduardo Delgado Paredes, Paulo Roberto Delgado Rojas, Consuelo Rojas Idrogo

Licencia de Creative Commons
Esta obra está bajo una licencia de Creative Commons Reconocimiento-NoComercial 4.0 Internacional.