POTENTIAL USES OF THE PEEL AND SEED OF PASSIFLORA EDULIS SIMS F. EDULIS (GULUPA) FROM ITS CHEMICAL CHARACTERIZATION, ANTIOXIDANT, AND ANTIHYPERTENSIVE FUNCTIONALITIES

LAURA GONZÁLEZ; ANDREE ÁLVAREZ; ELIZABETH MURILLO; CARLOS GUERRA; JONH MÉNDEZ

doi:10.22159/ajpcr.2019.v12i10.33828

Authors

LAURA GONZÁLEZ Department Chemistry, Natural Products Research Group (GIPRONUT), Science School, University of Tolima, Ibagué, Colombia.
ANDREE ÁLVAREZ Department Chemistry, Natural Products Research Group (GIPRONUT), Science School, University of Tolima, Ibagué, Colombia.
ELIZABETH MURILLO Department Chemistry, Natural Products Research Group (GIPRONUT), Science School, University of Tolima, Ibagué, Colombia.
CARLOS GUERRA Department Chemistry, Natural Products Research Group (GIPRONUT), Science School, University of Tolima, Ibagué, Colombia.
JONH MÉNDEZ Department Chemistry, Natural Products Research Group (GIPRONUT), Science School, University of Tolima, Ibagué, Colombia.

DOI:

https://doi.org/10.22159/ajpcr.2019.v12i10.33828

Keywords:

Gulupa, Passiflora, Antioxidant, Antihypertensive activity, Agroindustrial residues

Abstract

Objective: Assess the performance of a crude ethanolic extract, a dichloromethane fraction and a hydroalcoholic residue, which are the basis for chemically and biologically characterizing the husk and seed of Passiflora edulis f. edulis, collected in the region and Colombia with a view to determining potential uses.

Methods: Agroindustrial residues of gulupa (peel and seed) were analyzed through a bromatological study; subsequently, they were macerated with ethanol (96%). The crude ethanolic extract was partitioned with dichloromethane, leaving a hydroalcoholic residue. The content of total phenols, the composition of phytophenols (high-performance liquid chromatography-mass spectrometry), the total antioxidant capacity using 3-ethyl benzothiazoline-6-sulfonic acid (ABTS●+) and 2,2-diphenyl-1-pyridyl hydrazyl (DPPH●), the oxygen radical absorbance capacity (ORAC), and the ferric reduction power (FRAP) were determined to the extract, the fraction, and the residue. The evaluation of the inhibitory activity of the angiotensin-converting enzyme inhibitor (ACEI) and the cell viability assay with diphenyl bromide 3- (4,5-dimethylthiazole-2-) il) -2,5-tetrazolium on human leukocytes complemented the characterization.

Results: Agroindustrial waste of P. edulis f. edulis, peel and seed, contains as main constituents: Protein (8.49 and 7.29%), fiber (34.2 and 55.7%), phosphorus (1.67 and 3.09), and boron (53.3 and 58.4 mg/kg), respectively. The seed showed 25.5% oil. The crude seed extract exhibited a higher phenolic content (15.34 gEAG/100 g). Likewise, it presented the highest antiradical capacity against ABTS●+ and DPPH● (706.17 and 82.81 trolox equivalent antioxidant capacity [TEAC], respectively) and antioxidant in ORAC and FRAP (142.79 TEAC and 103.63 equivalent ascorbic acid EAA, respectively). The ACEI activity (50% inhibitory concentration 17.62 mg/L) of the crude seed extract was higher than the other samples. No toxicity was found in the samples evaluated at concentrations higher than those of the biological activities manifested.

Conclusion: The agroindustrial residues of P. edulis f. edulis (peel and seed) are rich in nutrients, which propose them for use in food matrices. The ethanolic extract from seed showed the highest antioxidant, antiradical, and inhibitory biological activity of the ACEI so that it could be proposed the gulupa seed as a promising phytotherapeutic product associated with its phenolic content, especially its flavonoids. The results obtained allow an added value to the fruit, reducing the chances that its waste contributes to environmental pollution.

Downloads

Download data is not yet available.

References

Ocampo J, Wyckhuys K. Tecnología Para el Cultivo de la Gulupa en Colombia (Passiflora edulis f. edulis Sims). Purple Passion Fruit. Colombia: Universidad Jorge Tadeo Lozano; 2012.

Gobierno de Colombia and Minagricultura. Informe de la Cadena de Pasifloras; 2018. Available from: http://www.fedepasifloras. org/es/wp-content/uploads/2018/01/Libro-memorias-III-Congreso- Latinoamericano-y-I-Congreso-Mundial-de-Pasifloras-2017.pdf.

Orjuela N, Campos S, Sánchez J, Melgarejo L, Hernández M. Manual de Manejo Poscosecha de la Gulupa (Passiflora edulis Sims). Poscosecha la Gulupa (Passiflora edulis Sims); 2011. p. 7-22. Available from: http://www.bdigital.unal.edu.co/8532/3/03_Cap01.pdf.

Pérez JO, d’Eeckenbrugge GC, Restrepo M, Jarvis A, Salazar M, Caetano C. Diversity of Colombian Passifloraceae: Biogeography and an updated list for conservation. Biota Colomb 2007;8:1-45.

Méndez-Arteaga JJ, Murillo-Perea E, Sabogal-Palma AC, Chávez- Marín J. Funcionalidades biológicas de Passiflora maliformis del sur macizo Colombiano. Bioagro 2016;28:3-12.

Chavez J, Sabogal A. Caracterización Física, Química y Funcionalidad Biológica de tres Pasifloras del Sur Macizo Colombiano y su Potencial Aplicación en la Agroindustria; 2014.

Fischer G, Montaño A, Pachón A. Efecto del empaque, encerado y temperatura sobre las características fisicoquímicas y organolépticas de la gulupa (Passiflora edulis f. edulis) en postcosecha. In: Propiedades Fisicoquímicas y Sistemas de procesado: Productos Hortofrutícolas en el Desarrollo Agroalimentario. Bogotá: Editora Guadalupe; 2015.

Pinzón IM, Fisher G, Corredor G. Determination of the maturity stages of purple passion fruit. Agron Colomb 2007;25:83-95.

Corrêa RC, Peralta RM, Haminiuk CW, Maciel GM, Bracht A, Ferreira IC. The past decade findings related with nutritional composition, bioactive molecules and biotechnological applications of Passiflora spp. (passion fruit). Trends Food Sci Technol 2016;58:79-95.

Yockteng R, d’Eeckenbrugge GC, Souza-chies TT. Passiflora. In: Kole C, editor. Wild Crop Relatives: Genomic and Breeding Resources. Berlin, Heidelberg: Springer; 2011.

Li H, Zhou P, Yang Q, Shen Y, Deng J, Li L, et al. Comparative studies on anxiolytic activities and flavonoid compositions of Passiflora edulis “edulis” and Passiflora edulis “flavicarpa”. J Ethnopharmacol 2011;133:1085-90.

Quintero-López J. Fracciones Polares y Apolares del Extracto Etanólico de Hojas de Passiflora edulis; 2017. p. 1-63.

Armas JP. Estudio Preclínico y Clínico de la Seguridad y Actividad Antihipertensiva de Passiflora edulis Sims (maracuyá); 2009. Available from: http://www.cybertesis.unmsm.edu.pe/handle/cybertesis/790.

Tiwari S, Singh S, Tripathi S, Kumar S. A pharmacological review: Passiflora species. Int J Pharmacogn 2016;3:10-8.

Calle AF. Extracción, Caracterización por CG-EM y Actividad Antibacteriana del Aceite Esencial Obtenido Mediante Hidrodestilación de Passiflora edulis flavicarpa de Origen Ecuatoriano; 2015.

Jurado-Mejía AG. In: Vera MS, Duque FM, Castorena PH, Peñaranda ML, Quevedo MS, editors. Una Estrategia de Desarrollo Agroindustrial Sostenible en Territorio de Paz. Florencia, Caquetá, Colombia; 2016.

Corporación Colombia Digital. Diagnóstico General Municipio de Cajamarca. Cajamarca: Corporación Colombia Digital; 2019.

Association of Official Analytical Chemists. Official Methods of Analysis. 16th ed. Washington DC, USA: Association of Official Analytical Chemists; 1995.

Harborne JB. Phytochemical Methods. New York: McGraw-Hill; 1980. P. 34-226.

Kusmardiyani S, Novita G, Fidrianny I. Antioxidant activities from various extracts of different parts of kelakai (Stenochlaena palustris) grown in central Kalimantan Indonesia. Asian J Pharm Clin Res 2016;9:215-9.

Palomino G, Lady R, García PC, Gil GJ, Rojano AB, Durango RD. Determinación del contenido de fenoles y evaluación de la actividad antioxidante de propóleos recolectados en el departamento de antioquia (Colombia). Vitae 2009;63:388-95.

Delpino-Rius A, Eras J, Vilaró F, Cubero MÁ, Balcells M, Canela- Garayoa R, et al. Characterisation of phenolic compounds in processed fibres from the juice industry. Food Chem 2015;172:575-84.

Braca A, Sortino C, Politi M, Morelli I, Mendez J. Antioxidant activity of flavonoids from Licania licaniaeflora. J Ethnopharmacol 2002;79:379-81.

Marquina V, Araujo L, Ruíz J, Rodríguez-Malaver A, Vit P. Composición química y capacidad antioxidante en fruta, pulpa y mermelada de guayaba (Psidium guajava L.). Arch Latinoam Nutr 2008;58:98-102.

UASLP Avenida Venustiano Carranza. Laboratorio de Genómica Viral y Humana Facultad de Medicina Universidad Autonoma de. Aislamiento de Células Mononucleares Humanas por Gradiente de Ficoll. San Luis Potosi: UASLP Avenida Venustiano Carranza; 2013. p. 1-4.

Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63.

Patel S, Gheewala N, Suthar A, Shah A. In-vitro cytotoxicity activity of Solanum nigrum extract against hela cell line and vero cell line. Int J Pharm Pharm Sci 2015;1:38-46.

Adeyeye E, Ekiti A, Aremu MO. Chemical composition of the raw fruit coat, seed and pulp of passion fruit (Passiflora edulis). Trends Sci Technol J 2017;2:334-41.

Badui S. Química de los Alimentos. México, DF: Cuarta; 2006. p. 736.

Belitz H, Grosch W. Química de los Alimentos. Zaragosa España: Acribia; 1997. p. 1087.

Perez-Cortéz S, Tillett S, Escalla M. Estudio morfológico de la semilla de 51 especies del género Passiflora L. Acta Bot Venez 2002;25:67-96.

Matilla A. Desarrollo y germinación de las semillas. In: Azcón-Bieto JJ, Talón M, editors. Fundamentos de Fisiología Vegetal. McGraw Hill; 2008. p. 1-39. Available from: https://www.researchgate.net/ publication/271512205_Desarrollo_y_germinacion_de_las_semillas.

Doria J. Revisión bibliográfica generalidades sobre las semillas : Su producción, conservación y almacenamiento. Cultiv Trop 2010;31:74 85.

Carvajal-De pabón LM, Turbay S, Álvarez L, Rodríguez A, Álvarez JM, Bonilla K, et al. (Passiflora ligularis Juss) Y su composición fitoquímica relationship between relación entre los usos populares de la granadilla (Passiflora ligularis Juss). Y relationship between the folk uses of the granadilla plant (Passiflora ligularis Juss) and its phytoche. Biotecnol Sect Agropecu Agroind 2014;12:185-96.

Salgado JM, Aparecida T, Bombarde D, Mansi DN, Maria S, Piedade DS, et al. Effects of different concentrations of passion fruit peel (Passiflora edulis) on the glicemic control in diabetic rat. Ciên Tecnol Aliment 2010;30:784-9.

Carvajal-De pabón LM, Turbay S, Álvarez L, Rodríguez A. Functional and nutritional properties of six species of Passiflora (Passifloraceae) from the department of Huila, Colombia. Caldasia 2014;36:1-15.

Deshmukh N, Patel R, Okram S, Banga U, Vishwavidyalaya K, Rymbai H. Passion fruit (Passiflora spp.). In: Ghosh SN, Singh A, Thakur A, editors. Underutilized Fruit Crops: Importance and Cultivation PART-II. 1st ed. New Delhi: Jaya Publishing House; 2017. p. 27.

Cassia R, Neuza J. Yellow passion fruit seed oil (Passiflora edulis f. flavicarpa): Physical and chemical characteristics. Braz Arch Biol Technol 2012;55:127-34.

Chóez-guaranda I, Ortega A, Miranda M, Manzano P. Chemical composition of essential oils of Passiflora edulis f. flavicarpa agroindustrial waste. Emirates J Food Agric 2017;29:458-62.

Regis SA, de Resende ED, Antoniassi R. Oil quality of passion fruit seeds subjected to a pulp-waste purification process. Ciên Rural 2015;45:977-84.

Cerón AF, Osorio O, Hurtado A. Identificación de ácidos grasos contenidos en los aceites extraídos a partir de semillas de tres diferentes especies de frutas. Acta Agron 2012;61:126-32.

Silva R, Placido G, Silva M, Castro C, LIma M, Caliari M. Chemical characterization of passion fruit (Passiflora edulis f. flavicarpa) seeds. Afr J Biotechnol 2016;14:1230-3.

International Plant Nutrition Institute. Functions of phosphorus in plants. Better Crop 1999;83:6-7.

International Plant Nutrition Institute. Phosphorus in animal nutrition. Better Crop 1999;83:32-3.

Urango-Anaya K, Ortega-Quintana F, Vélez-Hernández G, Pérez-Sierra Ó. Rapid extraction of pectin from passion fruit peel (Passiflora edulis flavicarpa) using microwave. Inf Tecnol 2018;29:129-36.

Ahmad W, Kanwal S. Role of boron in plant growth : A review. J Agric Res 2009;43:329-38.

Cooman A, Torres C, Fischer G. Determinación de las causas del rajado del fruto de uchuva (Physalis peruviana L.) bajo cubierta. II. Efecto de la oferta de calcio, boro y cobre. Agron Colomb 2005;23:74-82.

Jukanti A. Polyphenol Oxidases (PPOs) in Plants. Berlin: Springer; 2017.

Newman DJ, Cragg GM. Natural products as sources of new drugs over the last 25 years. J Nat Prod 2007;70:461-77.

Liu RH. Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals. Am J Clin Nutr 2003;78:517S-520S.

Talcott ST, Percival SS, Pittet-Moore J, Celoria C. Phytochemical composition and antioxidant stability of fortified yellow passion fruit (Passiflora edulis). J Agric Food Chem 2003;51:935-41.

Lourith N, Kanlayavattanakul M. Antioxidant activities and phenolics of Passiflora edulis seed recovered from juice production residue. J Oleo Sci 2013;62:235-40.

Konta EM, Almeida MR, do Amaral CL, Darin JD, de Rosso VV, Mercadante AZ, et al. Evaluation of the antihypertensive properties of yellow passion fruit pulp (Passiflora edulis sims f. flavicarpa Deg.) in spontaneously hypertensive rats. Phytother Res 2014;28:28-32.

Ribas C, Corrêa B, Pereira L, Rodrigues M, Ferreira E, da Silveira S, et al. Ethanolic extract of Passiflora edulis Sims leaves inhibits protein glycation and restores the oxidative burst in diabetic rat macrophages after Candida albicans exposure. Braz J Pharm Sci 2015;51:869-78.

Otify A, George C, Elsayed A, Farag MA. Mechanistic evidence of Passiflora edulis (Passifloraceae) anxiolytic activity in relation to its metabolite fingerprint as revealed via LC-MS and chemometrics. Food Funct 2015;6:3807-17.

Soulimani R, Younos C, Jarmouni S, Bousta D, Misslin R, Mortier F, et al. Behavioural effects of Passiflora incarnata L. and its indole alkaloid and flavonoid derivatives and maltol in the mouse. J Ethnopharmacol 1997;57:11-20.

Zeraik ML, Pereira CA, Zuin VG, Yariwake JH. Maracujá : Um alimento funcional ? Revisão. Rev Bras Farmacogn 2010;20:459-71.

Di Gioia F, Petropoulos SA. Phytoestrogens, phytosteroids and saponins in vegetables: Biosynthesis, functions, health effects and practical applications. Adv Food Nutr Res 2019;90:351-421.

Loyola-vargas VM, Sánchez-iturbe P, Canto-canché B, Gutiérrez- pacheco LC, Moreno-valenzuela O, Galaz-Ávalos R. Biosíntesis de los alcaloides indólicos. Una revisión crítica. J Mex Chem Soc 2004;48:67 94.

Fiallo VF, Lemes C, Rodríguez C, Sánchez P, Méndez G. Instructivo técnico del cultivo de Passiflora incarnata L. Rev Cuba Plantas Med 2000;5:118-22.

Moreno E, Ortiz BL, Restrepo LP. Total phenolic content and antioxidant activity of pulp extracts of six tropical fruits. Rev Colomb Quim 2014;43:41-8.

Marroquín MN, Cruz SM, Cáceres A. Antioxidant activity and phenolic compounds in three species of Passifloraceae (Passiflora edulis, P. incarnata, P. ligularis) from Guatemala. Acta Hortic 2012;964:93-8.

Charan SM, Gomez S, Sheela KB, Joseph PM, Sruthi CV. Quality characteristics and antioxidant activity of passion fruit (Passiflora edulis Sims.) accessions. Indian J Hortic 2018;75:185-90.

Pineli Lde L, Rodrigues Jda S, Costa AM, de Lima HC, Chiarello MD, Melo L, et al. Antioxidants and sensory properties of the infusions of wild Passiflora from Brazilian savannah: Potential as functional beverages. J Sci Food Agric 2015;95:1500-6.

Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 2006;160:1-40.

Xie J, Schaich KM. Re-evaluation of the 2,2-diphenyl-1-picrylhydrazyl free radical (DPPH) assay for antioxidant activity. J Agric Food Chem 2014;62:4251-60.

Carvajal LM, Turbay S, Rojano B, Álvarez LM, Restrepo SL, Álvarez JM, et al. Algunas especies de Passiflora y su capacidad antioxidante. Rev Cuba Plantas Med 2011;16:354-63.

Rojano BA, Zapata K, Correa FB. Capacidad atrapadora de radicales libres de Passiflora mollissima (Kunth) L. H. Bailey (curuba). Rev Cuba Plantas Med 2012;17:408-19.

Navarro SA, Aldana AP, Longas FF. Potencial antioxidante y antimicrobiano de extractos acuosos e hidroalcohólicos de granadilla (Passiflora ligularis). Acta Agron 2014;63:204-11.

Duran M, Montero P, Marrugo Y. Extractos metanólicos de corteza de guayaba (Psidium guajava L.) y mango (Mangifera indica L.): Efecto citotóxico, antihemolítico y en la morfología de membrana de eritrocitos. Rev UDCA Actual Divulg Cient 2013;16:327-34.

Ebrahimzadeh MA, Safdari Y, Khalili M. Antioxidant activity of different fractions of methanolic extract of the golden chanterelle mushroom Cantharellus cibarius (Higher basidiomycetes) from iran. Int J Med Mushrooms 2015;17:557-65.

Ebrahimzadeh MA, Nabavi SM, Nabavi SF, Bahramian F, Bekhradnia AR. Antioxidant and free radical scavenging activity of H. officinalis L. var. angustifolius, V. odorata, B. hyrcana and C. speciosum. Pak J Pharm Sci 2010;23:29-34.

Salazar-Aranda R, de la Torre-Rodríguez Y, Alanís-Garza B, Pérez- López LA, Waksman-de-Torres N. Evaluación de la actividad biológica de productos herbolarios comerciales. Med Univ 2009;44:156-64.

Tagle R. Diagnóstico de hipertensión arterial. Rev Méd Clín Condes 2018;29:12-20.

Quintero-López J. Inhibición de la enzima convertidora de angiotensina por las fracciones polares y apolares del extracto etanólico de hojas de Passiflora edulis. 2017.

Guerrero L, Castillo J, Quiñones M, Garcia-Vallvé S, Arola L, Pujadas G, et al. Inhibition of angiotensin-converting enzyme activity by flavonoids: Structure-activity relationship studies. PLoS One 2012;7:e49493.

Gosmann G, Provensi G, Comunello LN, Rates SM. Composição química e aspectos farmacológicos de espécies de Passiflora L. (Passifloraceae). Rev Bras Biociências 2011;9:88-99.

Rojas J, Ronceros S, Palomino R, Tomás G, Chenguayen J. Efecto antihipertensivo y dosis letal 50 del jugo del fruto y del extracto etanólico de las hojas de Passiflora edulis (maracuyá), en ratas. An Fac Med 2006;67:206-13.

Duarte J, Pérez-Palencia R, Vargas F, Ocete MA, Pérez-Vizcaino F, Zarzuelo A, et al. Antihypertensive effects of the flavonoid quercetin in spontaneously hypertensive rats. Br J Pharmacol 2001;133:117-24.

Carlström M, Lundberg JO, Weitzberg E. Mechanisms underlying blood pressure reduction by dietary inorganic nitrate. Acta Physiol (Oxf) 2018;224:e13080.

Duarte J, Pérez-vizcaíno F. Protección cardiovascular con flavonoides. Enigma farmacocinético cardiovascular protection by flavonoids. Pharmacokinetic mystery. Ars Pharm 2015;56:193-200.

Clin N, Sánchez-Rodríguez ME, Mesa MD, Sánchez-Rodríguez E, María C, Mesa García D. Compuestos bioactivos del aceite de oliva virgen. Nutr Clin Med 2018;12:80-94.

Yalcin E, Geli B. Antioxidant activity of cereal protein hydrolysates. Eur Food Res Technol 2010;35:227-33.

Queiroz F, Mota BC, Leite MN, Fonseca JM, Oliveira DA, De Andrade Royo V, et al. In vivo analgesic activity, toxicity and phytochemical screening of the hydroalcoholic extract from the leaves of Psidium cattleianum Sabine. J Ethnopharmacol 2013;150:280-4.

Rodríguez-Feo JA, Gómez J, Núñez A, Rico L, Fortes J, de Andrés R, et al. Doxazosina y guanilato ciclasa soluble en un modelo de ratas hipertensas. Rev Española Cardiol 2001;54:880-6.

Okonogi S, Duangrat C, Anuchpreeda S. Comparison of antioxidant capacities and cytotoxicities of certain fruit peels. Food Chem 2007;103:839-46.

Silva DC, Lucia A, Freitas P, Clark F, Barros N, Lins KO, et al. Polysaccharide isolated from Passiflora edulis : Characterization and antitumor properties. Carbohydr Polym 2012;87:139-45.S