Abstract
An antifungal coating of zein nanofibers with jackfruit leaf extract was successfully elaborated by electrospinning. The nanofibers were characterized based on thickness, tensile test, water vapor permeability, water solubility, differential scanning calorimetry, thermogravimetric analysis, scanning electron microscopy, and presumptive identification of some compounds in the extract and fibers with extract by HPLC-Masses. The average diameter of the pure nanofibers was 305 nm and for the nanofibers with extract was 731 nm. An encapsulation efficiency of 72% was obtained. FTIR results demonstrated that the jackfruit leaf extract was successfully encapsulated in the zein fibers and did not show strong chemical interactions with the extract. The TGA analysis showed that the zein fibers offered thermoprotection to the compounds in the extract. Inhibition of mycelial growth and spore germination of jackfruit leaf extract against Cladosporium tenuissimum and Aspergillus sydowii in vitro showed good results which were attributed to the antimicrobial activity of some phenolic compounds in the extract such as caffeic acid, kaempferol 3–O– rutinoside, and catechin. The preventive and curative treatments evaluated with the application of the nanofibers showed a decrease in the severity and incidence in the infected Averrhoa carambola L. fruits. The results indicate the encapsulation of the jackfruit leaf extract, as well as the thermoprotection and release of antimicrobial compounds from this matrix.
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Mateus-Cagua D, Arias Cruz ME, Orduz-Rodríguez JO (2015) Growing starfruit (Averrhoa carambola L.) and its behavior in the piedmont of Meta (Colombia) A review. Rev Colomb Ciencias Hortícolas. 9:135. https://doi.org/10.17584/rcch.2015v9i1.3752
Manda H, Vyas K, Pandya A, Singhal G (2012) A complete review on: Averrhoa carambola. World J Pharm Pharm Sci 1:17–33
Landero Valenzuela N, Lara Viveros FM, Andrade Hoyos P, Alfonso L, Graciano AP, Rodríguez JA (2016) Alternativas para el control de Colletotrichum spp. Alternatives for the control of Colletotrichum spp. Rev Mex Ciencias Agric 7:1189–1198
Díaz-Vallejo J, Barraza-Villarreal A, Yáñez-Estrada L, Hernández-Cadena L (2021) Plaguicidas en alimentos: riesgo a la salud y marco regulatorio en Veracruz México. Salud Publica Mex 63:486–497. https://doi.org/10.21149/12297
Villa-Martínez A, Pérez-Leal R, Morales-Morales HA, Ba-Surto-Sotelo M, Soto-Parra JM, Martínez-Escudero E (2014) Current situation of Fusarium spp in the control and evaluation of the an-tifungal activity on vegetables extracts. Acta Agron 64:194–205. https://doi.org/10.15446/acag.v64n2.43358
Huang HW, Hsu CP, Yang BB, Wang CY (2013) Advances in the extraction of natural ingredients by high pressure extraction technology. Trends Food Sci Technol 33:54–62. https://doi.org/10.1016/j.tifs.2013.07.001
Vázquez-González Y, Ragazzo-Sánchez JA, Calderón-Santoyo M (2020) Characterization and antifungal activity of jackfruit (Artocarpus heterophyllus Lam.) leaf extract obtained using conventional and emerging technologies. Food Chem 330:127211. https://doi.org/10.1016/j.foodchem.2020.127211
Aguilar-Veloz LM, Calderón-Santoyo M, Carvajal-Millan E, Martínez-Robinson K, Ragazzo-Sánchez JA (2022) Artocarpus heterophyllus Lam. Leaf extracts added to pectin-based edible coating for Alternaria sp. control in tomato. LWT-Food Sci Technol 156:113022. https://doi.org/10.1016/j.lwt.2021.113022
Gómez-Mascaraque LG, Tordera F, Fabra MJ, Martínez-Sanz M, Lopez-Rubio A (2019) Coaxial electrospraying of biopolymers as a strategy to improve protection of bioactive food ingredients. Innov Food Sci Emerg Technol 51:2–11. https://doi.org/10.1016/j.ifset.2018.03.023
Raybaudi-Massilia RM, Tapia MS, Mosqueda-Melgar J (2013) Películas y recubrimientos comestibles con efecto antimicrobiano. In: Olivas Orozco GI, González-Aguilar GA, Martín-Belloso O, Soliva-Fortuny R. Películas y recubrimientos comestibles. Propiedades y aplicaciones en alimentos, CIAD, México, 329–361
Iñiguez-Moreno M, Ragazzo-Sánchez JA, Calderón-Santoyo M (2021) An extensive review of natural polymers used as coatings for postharvest shelf-life extension: trends and challenges. Polymers 13:13193271. https://doi.org/10.3390/polym13193271
Bean SR, Akin PA, Aramouni FM (2021) Zein functionality in viscoelastic dough for baked food products. J Cereal Sci 100:103270. https://doi.org/10.1016/j.jcs.2021.103270
Suganya P, Vaseeharan B, Vijayakumar S, Balan B, Govindarajan M, Alharbi NS, Kadaikunnan S, Khaled JM, Benelli G (2017) Biopolymer zein-coated gold nanoparticles: synthesis, antibacterial potential, toxicity and histopathological effects against the Zika virus vector Aedes aegypti. J Photochem Photobiol B Biol 173:404–411. https://doi.org/10.1016/j.jphotobiol.2017.06.004
Chiralt A, Fabra MJ, Sánchez-González L (2013) Propiedades de las películas comestibles. In: Olivas Orozco GI, González-Aguilar GA, Martín-Belloso O, Soliva-Fortuny R. Películas y recubrimientos comestibles. Propiedades y aplicaciones en alimentos, CIAD, México, 21–57
Pant HR, Park CH, Tijing LD, Amarjargal A, Lee DH, Kim CS (2012) Bimodal fiber diameter distributed graphene oxide/nylon-6 composite nanofibrous mats via electrospinning. Colloids Surfaces A Physicochem Eng Asp 407:121–125. https://doi.org/10.1016/j.colsurfa.2012.05.018
Torres-Giner S, Wilkanowicz S, Melendez-Rodriguez B, Lagaron JM (2017) Nanoencapsulation of aloe vera in synthetic and naturally occurring polymers by electrohydrodynamic processing of interest in food technology and bioactive packaging. J Agric Food Chem 65:4439–4448. https://doi.org/10.1021/acs.jafc.7b01393
Alehosseini A, Sarabi-Jamab M, Ghorani B, Kadkhodaee R (2019) Electro-encapsulation of Lactobacillus casei in high-resistant capsules of whey protein containing transglutaminase enzyme. LWT-Food Sci Technol 102:150–158. https://doi.org/10.1016/j.lwt.2018.12.022
Drosou CG, Krokida MK, Biliaderis CG (2017) Encapsulation of bioactive compounds through electrospinning/electrospraying and spray drying: a comparative assessment of food-related applications. Dry Technol 35:139–162. https://doi.org/10.1080/07373937.2016.1162797
Gonzales Molfino HM, Alcalde Yañez A, Valverde Morón VV, Villanueva Salvatierra DV (2020) Electrospinning: advances and applications in the field of biomedicine. Rev Fac Med Humana 20:706–713. https://doi.org/10.25176/rfmh.v20i4.3004
Millán EE, Macanás de Benito J, Carrillo Navarrete F (2018) Preparación de soportes biomateriales de naturaleza proteica mediante electrohilatura. Afinidad 75(582):83–90
Iñiguez-Moreno M, Ragazzo-Sánchez JA, Barros-Castillo JC, Solís-Pacheco JR, Calderón-Santoyo M (2021) Characterization of sodium alginate coatings with Meyerozyma caribbica and impact on quality properties of avocado fruit. LWT-Food Sci Technol 152:112346. https://doi.org/10.1016/j.lwt.2021.112346
Costa AS, Ribeiro LR, Koblitz MGB (2011) Uso de atmosfera controlada e modificada em frutos climatéricos e não-climatéricos. SITIENTIBUS série Ciências Biológicas 11:1–7. https://doi.org/10.13102/scb139
Calderón-Santoyo M, Iñiguez-Moreno M, Ragazzo-Sánchez JA (2022) Microencapsulation of citral and its antifungal activity into pectin films. Biointerface Res Appl Chem 12:7488–7502. https://doi.org/10.33263/BRIAC126.74887502
Trinidad-Ángel E, Ascencio-Valle FJ, Ulloa JA, Ramírez-Ramírez JC, Ragazzo-Sánchez JA, Calderón-Santoyo M, Bautista Rosales PU (2017) Identification and characterization of Colletotrichum spp. causing anthracnose in avocado Nayarit, Mexico. Rev Mex Ciencias Agric 8(spe19):3953–3964. https://doi.org/10.29312/remexca.v0i19.664
Páramo-Aguilera L, Ortega-Morales BO, Narváez-Zapata JA (2012) Culturable fungi associated with urban stone surfaces in Mexico City. Electron J Biotechnol. https://doi.org/10.2225/vol15-issue4-fulltext-6
Campos-Rivero G, Sánchez-Teyer LF, De la Cruz-Arguijo EA, Ramírez-González MS, Larralde-Corona CP, Narváez-Zapata JA (2019) Bioprospecting for fungi with potential pathogenic activity on leaves of Agave tequilana Weber var. Azul J Phytopathol 167:283–294. https://doi.org/10.1111/jph.12797
González-Estrada RR, Carvajal-Millán E, Ragazzo-Sánchez JA, Bautista-Rosales PU, Calderón-Santoyo M (2017) Control of blue mold decay on Persian lime: application of covalently cross-linked arabinoxylans bioactive coatings with antagonistic yeast entrapped. LWT-Food Sci Technol 85:187–196. https://doi.org/10.1016/j.lwt.2017.07.019
Murrieta-Martínez C, Soto-Valdez H, Pacheco-Aguilar R, Torres-Arreola W, Rodríguez-Felix F, Ramírez-Wong B, Santacruz-Ortega H, Santos-Sauceda I, Olibarría-Rodríguez G, Márquez-Ríos E (2019) Effect of different polyalcohols as plasticizers on the functional properties of squid protein film (Dosidicus Gigas). Coatings 9:77. https://doi.org/10.3390/coatings9020077
Maria Leena M, Yoha KS, Moses JA, Anandharamakrishnan C (2020) Edible coating with resveratrol loaded electrospun zein nanofibers with enhanced bioaccessibility. Food Biosci 36:100669. https://doi.org/10.1016/j.fbio.2020.100669
Le NT, Myrick JM, Seigle T, Huynh PT, Krishnan S (2018) Mapping electrospray modes and droplet size distributions for chitosan solutions in unentangled and entangled concentration regimes. Adv Powder Technol 29:3007–3021. https://doi.org/10.1016/j.apt.2018.10.006
Ali R et al (2020) Electrospinning/electrospraying coatings for metal microneedles: a design of experiments (DOE) and quality by design (QbD) approach. Eur J Pharm Biopharm 156:20–39. https://doi.org/10.1016/j.ejpb.2020.08.023
Hoque MS, Benjakul S, Prodpran T (2011) Properties of film from cuttlefish (Sepia pharaonis) skin gelatin incorporated with cinnamon, clove and star anise extracts. Food Hydrocoll 25:1085–1097. https://doi.org/10.1016/j.foodhyd.2010.10.005
Pandia-Estrada S, Romero-Santivañez R, Céspedes-Chombo R, Solari-Godiño A (2021) Edible films gelatin-based obtained from mahi-mahi skin (Coryphaena hippurus) and oregano extract: physicochemical, antimicrobial, structural and surface characteristics. Sci Agropecu 12:229–237. https://doi.org/10.17268/sci.agropecu.2021.026
Yue TT, Li X, Wang XX, Yan X, Yu M, Ma JW, Zhou Y, Ramakrishna S, Long YZ (2018) Electrospinning of carboxymethyl chitosan/polyoxyethylene oxide nanofibers for fruit fresh-keeping. Nanoscale Res Lett 13:239. https://doi.org/10.1186/s11671-018-2642-y
Debeaufort F, Voilley A (2009) Lipid-based edible films and coatings. In: Huber K, Embuscado M (eds) Edible Films and Coatings for Food Applications. Springer, New York
Xu Y, Yifu C, Feng X, Gao C, Wu D, Cheng W, Meng L, Zhang Y, Tang X (2020) Effects of zein stabilized clove essential oil Pickering emulsion on the structure and properties of chitosan-based edible films. Int J Biol Macromol 156:111–119. https://doi.org/10.1016/j.ijbiomac.2020.04.027
Torres-Giner S, Gimenez E, Lagaron JM (2008) Characterization of the morphology and thermal properties of Zein Prolamine nanostructures obtained by electrospinning. Food Hydrocoll 22:601–614. https://doi.org/10.1016/j.foodhyd.2007.02.005
Xu W, Karst D, Yang W, Yang Y (2008) Novel zein-based electrospun fibers with the water stability and strength necessary for various applications. Polym Int 57:1110–1117. https://doi.org/10.1002/pi.2450
Karim M, Fathi M, Soleimanian-Zad S (2020) Nanoencapsulation of cinnamic aldehyde using zein nanofibers by novel needle-less electrospinning: production, characterization and their application to reduce nitrite in sausages. J Food Eng 288:110140. https://doi.org/10.1016/j.jfoodeng.2020.110140
Dehcheshmeh MA, Fathi M (2019) Production of core-shell nanofibers from zein and tragacanth for encapsulation of saffron extract. Int J Biol Macromol 122:272–279. https://doi.org/10.1016/j.ijbiomac.2018.10.176
Bhushani JA, Kurrey NK, Anandharamakrishnan C (2017) Nanoencapsulation of green tea catechins by electrospraying technique and its effect on controlled release and in-vitro permeability. J Food Eng 199:82–92. https://doi.org/10.1016/j.jfoodeng.2016.12.010
Gomez-Estaca J, Balaguer MP, Gavara R, Hernandez-Munoz P (2012) Formation of zein nanoparticles by electrohydrodynamic atomization: Effect of the main processing variables and suitability for encapsulating the food coloring and active ingredient curcumin. Food Hydrocoll 28:82–91. https://doi.org/10.1016/j.foodhyd.2011.11.013
Miss-Zacarías DM, Iñiguez-Moreno M, Calderón-Santoyo M, Ragazzo-Sánchez JA (2020) Optimization of ultrasound-assisted microemulsions of citral using biopolymers: characterization and antifungal activity. J Dispers Sci Technol. https://doi.org/10.1080/01932691.2020.1857264
Yang M, Shi J, Xia Y (2018) Effect of SiO2, PVA and glycerol concentrations on chemical and mechanical properties of alginate-based films. Int J Biol Macromol 107:2686–2694. https://doi.org/10.1016/j.ijbiomac.2017.10.162
O’Neil MJ (2001) The Merck Index–An Encyclopedia of Chemicals, Drugs, and Biologicals, In: 13th ed.Cambridge: Royal Society of Chemistry, New Jersey, EU
Cheng M, Wang J, Zhang R, Kong R, Lu W, Wang X (2019) Characterization and application of the microencapsulated carvacrol/sodium alginate films as food packaging materials. Int J Biol Macromol 141:259–267. https://doi.org/10.1016/j.ijbiomac.2019.08.215
Abbehausen C, Formiga ALB, Sabadini E, Yoshida IVP (2010) A b-cyclodextrin/siloxane hybrid polymer: synthesis, characterization and inclusion complexes. J Braz Chem Soc 21:1867–1876. https://doi.org/10.1590/S0103-50532010001000011
Ben ST, Belsey S, Chasnitsky M, Shoseyov O (2021) Cellulose nanocrystals and corn zein oxygen and water vapor barrier biocomposite films. Nanomaterials 11:1–16. https://doi.org/10.3390/nano11010247
Yang H, Feng K, Wen P, Zong MH, Lou WY, Wu H (2017) Enhancing oxidative stability of encapsulated fish oil by incorporation of ferulic acid into electrospun zein mat. LWT-Food Sci Technol 84:82–90. https://doi.org/10.1016/j.lwt.2017.05.045
Okur İ, Baltacıoğlu C, Ağçam E, Baltacıoğlu H, Alpas H (2019) Evaluation of the effect of different extraction techniques on sour cherry pomace phenolic content and antioxidant activity and determination of phenolic compounds by FTIR and HPLC. Waste Biomass Valori 10:3545–3555. https://doi.org/10.1007/s12649-019-00771-1
Yao ZC, Chang MW, Ahmad Z, Li JS (2016) Encapsulation of rose hip seed oil into fibrous zein films for ambient and on demand food preservation via coaxial electrospinning. J Food Eng 191:115–123. https://doi.org/10.1016/j.jfoodeng.2016.07.012
De la Rosa LA, Álvarez-Parrilla E, García-Fajardo JA (2019) Identification of phenolic compounds in almond (Prunus dulcis) and pecan (Carya illinoinensis) extracts by liquid chromatography coupled to tandem mass spectrometry (HPLC-MS/MS). TIP Rev Esp Cienc Quím Biol 22:1–13. https://doi.org/10.22201/fesz.23958723e.2019.0.179
Olivas-Aguirre FJ, Wall-Medrano A, González-Aguilar GA, López-Díaz JA, Álvarez-Parrilla E, De la Rosa LA, Ramos-Jimenez A (2015) Taninos hidrolizables; bioquímica, aspectos nutricionales y analíticos y efectos en la salud. Nutr Hosp 31:55–66. https://doi.org/10.3305/nh.2015.31.1.7699
Elhawary SS, Younis IY, El Bishbishy MH, Khattab AR (2018) LC–MS/MS-based chemometric analysis of phytochemical diversity in 13 Ficus spp. (Moraceae): Correlation to their in vitro antimicrobial and in silico quorum sensing inhibitory activities. Ind Crops Prod 126:261–271. https://doi.org/10.1016/j.indcrop.2018.10.017
Hagerman AE (2012) Fifty years of polyphenol – protein complexes. In: Cheynier V, Sarni-Manchado P, Quideau S (eds) Recent Advances in Polyphenol Research. John Wiley & Sons Ltd, UK, pp 71–97. https://doi.org/10.1002/9781118299753.ch3
Dewick PM (2009) Medicinal natural products: a biosynthetic approach, 3rd edn. Wiley, New Jersey
Mesa VAM, Marín PA, Ocampo O, Calle J, Monsalve Z (2019) Fungicidas a partir de extractos vegetales: una alternativa en el manejo integrado de hongos fitopatógenos. Rev Investig Agropecu 45:23–30
Trumbeckaite S, Bernatoniene J, Majiene D, Jakštas V, Savickas A, Toleikis A (2006) The effect of flavonoids on rat heart mitochondrial function. Biomed Pharmacother 60:245–248. https://doi.org/10.1016/j.biopha.2006.04.003
Linares C, Quiñones-Gálvez J, Pérez Martínez AT, Carvajal Ortiz CC, Rivas Paneca M, Cid Valdéz GA, Pérez Gómez L, La Rosa GS, Capdesuñer Ruiz YK (2018) Obtención de extractos fenólicos foliares de Moringa oleifera Lam mediante el uso de diferentes métodos de extracción. Biotecnol Veg 18(1):47–56
Solano-Doblado LG, Alamilla-Beltrán L, Jiménez-Martínez C (2018) Películas y recubrimientos comestibles funcionalizados. TIP Rev Esp Cienc Quím Biol 21:30. https://doi.org/10.22201/fesz.23958723e.2018.0.153
Olivas-Orozco GI, Perez-Gago MB (2012) Películas y recubrimientos comestibles para frutas y verduras. In: Olivas Orozco GI, González-Aguilar GA, Martín-Belloso O, Soliva-Fortuny R. Películas y recubrimientos comestibles. In: Propiedades y aplicaciones en alimentos, CIAD, México, 385–412.
Balbuena Escalona V (2012) Evaluation of the antimicrobial effect of flavonoids obtained from the extracts of leaves of Tamarindus indica Lin. Mul Med 16(1):69–84
Vázquez-González Y, Prieto C, Stojanovic M, Torres CAV, Freitas F, Ragazzo-Sánchez JA, Calderón-Santoyo M, Lagaron JM (2022) Preparation and characterization of electrospun polysaccharide fucopol-based nanofiber systems. Nanomaterials 12:1–15. https://doi.org/10.3390/nano12030498
Sharma B, Kumar P (2009) In vitro antifungal potency of some plant extracts against Fusarium oxysporum. Int J Green Pharm 3:63–65. https://doi.org/10.4103/0973-8258.49377
Timóteo P, Karioti A, Leitão SG, Vincieri FF, Bilia AR (2015) A validated HPLC method for the analysis of herbal teas from three chemotypes of Brazilian Lippia alba. Food Chem 175:366–373. https://doi.org/10.1016/j.foodchem.2014.11.129
López-Cobo A, Gómez-Caravaca AM, Cerretani L, Segura-Carretero A, Fernández-Gutiérrez A (2014) Distribution of phenolic compounds and other polar compounds in the tuber of Solanum tuberosum L. by HPLC-DAD-q-TOF and study of their antioxidant activity. J Food Compos Anal 36:1–11. https://doi.org/10.1016/j.jfca.2014.04.009
Acknowledgements
The authors thank CONACYT for the scholarship number 808172 awarded to Karla Deyanira Ayón Macías to carry out this project, and Tecnologico Nacional de Mexico through the project 13838.22-P. This research was supported by CYTED network number 319RT0576.
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Ayón-Macías, K.D., Castañeda-Andrade, A.J., Ragazzo-Sánchez, J.A. et al. Application of nanofibers with jackfruit leaf extract via electrospinning to control phytopathogens in Averrhoa carambola L. Polym. Bull. 81, 2601–2626 (2024). https://doi.org/10.1007/s00289-023-04815-4
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DOI: https://doi.org/10.1007/s00289-023-04815-4