Sacha inchi (Plukenetia volubilis L.) husks and seed shells are sources of phenolic compounds with potential health benefits
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Dec 15, 2024
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Nicole Valeria Polanía Cuellar
https://orcid.org/0009-0004-0681-6673
Indira Paola Hernández Peñaranda
https://orcid.org/0000-0002-1305-8100
Deicy Villalba Rey
https://orcid.org/0000-0002-8579-1379
Katherin Natalia Acuña Rodríguez
https://orcid.org/0009-0005-1487-2568
Franci Nathalie Gómez Jaimes
https://orcid.org/0000-0001-8273-4013
https://orcid.org/0009-0004-0681-6673
Indira Paola Hernández Peñaranda
https://orcid.org/0000-0002-1305-8100
Deicy Villalba Rey
https://orcid.org/0000-0002-8579-1379
Katherin Natalia Acuña Rodríguez
https://orcid.org/0009-0005-1487-2568
Franci Nathalie Gómez Jaimes
https://orcid.org/0000-0001-8273-4013
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Abstract
Sacha inchi (Plukenetia volubilis L.) is an oilseed plant that yields a highly nutritious oil. However, its husks and seed shells are under-utilized byproducts. In this study, ethanolic extracts of sacha inchi husks (SI-husk) and seed shells (SI-shell) were obtained using ultrasound-assisted extraction, evaluating the effects of extraction temperature and solvent-to-solid ratio on the yields. The extracts’ total phenolic contents, phenolic profiles, antioxidant activities, and antimicrobial activities against Gram-positive and Gram-negative bacteria were investigated. Under the selected extraction conditions for SI-husk (60 °C, 1:8 s/s, 280W, 120 min) and SI-shell (60 °C, 1:3 s/s, 280W, 120 min), the extracts’ total phenolic contents were 80.18 ± 0.32 and 50.94 ± 0.48 mg GAE (gallic acid equivalents)/g, respectively. Cyanidin, naringenin, and kaempferol were principally found in the SI-husk extract (79.4 %) and vanillic acid in the SI-shell extract (79.9 %). Both extracts exhibited antioxidant activity, with ORAC values of 360.36 ± 0.21 and 228.11 ± 0.14 µmol TE/g, respectively. The antimicrobial activity of the extracts was evaluated against S. aureus, P. aeruginosa, and E. coli using the agar disk diffusion assay. SI-husk (1 mg) exhibited antibacterial activity against Staphylococcus aureus, with an inhibition zone of 10.5 ± 1.8 mm. Our results provide new insights into sacha inchi byproducts as sources of bioactive compounds with potential health benefits.
Keywords
antimicrobial; antioxidants; byproducts; oilseed; plant extracts; ultrasound.
References
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doi: 10.1016/j.cep.2020.107922
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doi: 10.14456/tjst.2020.30
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doi: 10.1039/D0FO01770A
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doi: 10.48048/tis.2023.6815
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doi: 10.3390/horticulturae8040344
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doi: 10.1016/j.jep.2015.06.009
[10] Wintachai P, Voravuthikunchai SP. Characterization of Novel Lytic Myoviridae Phage Infecting Multidrug-Resistant Acinetobacter baumannii and Synergistic Antimicrobial Efficacy between Phage and Sacha Inchi Oil, Pharmaceuticals, 15(3): 291, 2022.
doi: 10.3390/ph15030291
[11] Ampofo J, Ngadi M. Ultrasound-assisted processing: Science, technology and challenges for the plant-based protein industry, Ultrasonics Sonochemistry, 84: 105955, 2022.
doi: 10.1016/j.ultsonch.2022.105955
[12] Dastmalchi K, Damien-Dorman HJ, Koşar M, Hiltunen R. Chemical composition and in vitro antioxidant evaluation of a water-soluble Moldavian balm (Dracocephalum moldavica L.) extract, LWT, 40(2): 239–248, 2007.
doi: 10.1016/j.lwt.2005.09.019
[13] Ou B, Hampsch-Woodill M, Prior RL. Development and Validation of an Improved Oxygen Radical Absorbance Capacity Assay Using Fluorescein as the Fluorescent Probe, Journal of Agricultural and Food Chemistry, 49(10): 4619–4626, 2001.
doi: 10.1021/jf010586o
[14] Huang D, Ou B, Hampsch-Woodill M, Flanagan JA, Deemer EK. Development and Validation of Oxygen Radical Absorbance Capacity Assay for Lipophilic Antioxidants Using Randomly Methylated B-Cyclodextrin as the Solubility Enhancer, Journal of Agricultural and Food Chemistry, 50(7): 1815–1821, 2002.
doi: 10.1021/jf0113732
[15] CLSI. Performance standards for antimicrobial disk susceptibility tests: Approved standard, Clinical and Laboratory Standards Institute, 2012.
https://clsi.org/media/1631/m02a12_sample.pdf
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doi: 10.3390/pr8030322
[17] Hernández-Rodríguez P, Baquero LP, Larrota HR. Flavonoids: Potential Therapeutic Agents by Their Antioxidant Capacity, Bioactive Compounds: Health Benefits and Potential Applications; p. 265–288, 2018.
doi: 10.1016/B978-0-12-814774-0.00014-1
[18] Arias A, Feijoo G, Moreira MT. Exploring the potential of antioxidants from fruits and vegetables and strategies for their recovery, Innovative Food Science and Emerging Technologies, 77: 102974, 2022.
doi: 10.1016/j.ifset.2022.102974
[19] Santos-Sánchez NF, Salas-Coronado R, Villanueva-Cañongo C, Hernández-Carlos B. Antioxidant Compounds and Their Antioxidant Mechanism, Antioxidants. IntechOpen, 2019.
doi:10.5772/intechopen.85270
[20] Rakha A, Umar N, Rabail R, Butt MS, Kieliszek M, Hassoun A, Aadil RM. Anti-inflammatory and anti-allergic potential of dietary flavonoids: A review, Biomedicine & Pharmacotherapy, 156: 113945, 2022.
doi: 10.1016/j.biopha.2022.113945
[21] Zeb A. Concept, mechanism, and applications of phenolic antioxidants in foods, Journal of Food Biochemistry, 44(9): 1–22, 2020.
doi: 10.1111/jfbc.13394
[22] Khan A, Heng W, Wang Y, Qiu J, Wei X, Peng S, Saleem S, Khan M, Ali SS, Wei DQ. In silico and in vitro evaluation of kaempferol as a potential inhibitor of the SARS-CoV -2 main protease
(3CLpro), Phytotherapy Research, 35(6): 2841–2845, 2021.
doi: 10.1002/ptr.6998
[23] Tutunchi H, Naeini F, Ostadrahimi A, Hosseinzadeh-Attar MJ. Naringenin, a flavanone with antiviral and anti-inflammatory effects: A promising treatment strategy against COVID-19, Phytotherapy Research, 34(12): 3137–3147, 2020.
doi: 10.1002/ptr.6781
[24] Nascimento AKL, Melo-Silveira RF, Dantas-Santos N, Fernandes JM, Zucolotto SM, Rocha HAO, Scortecci KC. Antioxidant and Antiproliferative Activities of Leaf Extracts from Plukenetia volubilis Linneo (Euphorbiaceae), Evidence-Based Complementary and Alternative Medicine, 2013: 950272, 2013.
doi: 10.1155/2013/950272
[25] Vaou N, Stavropoulou E, Voidarou C, Tsigalou C, Bezirtzoglou E. Towards Advances in Medicinal Plant Antimicrobial Activity: A Review Study on Challenges and Future Perspectives, Microorganisms, 9(10): 2041, 2021.
doi: 10.3390/microorganisms9102041
[26] Adekola HA, Adeleye AO, Adesetan TO, Folorunso JB, Odeyemi FA. Antibacterial Activity of Vanillic Acid against Staphylococcus aureus, Salmonella typhi, and Proteus mirabilis, Microbes, Infection & Chemotherapy, 2(12): e1458, 2022.
doi: 10.54034/mic.e1548
[27] Resende FA, Nogueira LG, Bauab TM, Vilegas W, Varanda EA. Antibacterial potential of flavonoids with different hydroxylation patterns, Eclética Química Journal, 40(1): 173, 2015.
doi: 10.26850/1678-4618eqj.v40.1.2015.p173-179
[28] Veiko AG, Olchowik-Grabarek E, Sekowski S, Roszkowska A, Lapshina EA, Dobrzynska I, Zamaraeva M, Zavodnik IB. Antimicrobial Activity of Quercetin, Naringenin and Catechin: Flavonoids Inhibit Staphylococcus aureus-Induced Hemolysis and Modify Membranes of Bacteria and Erythrocytes, Molecules, 28(3): 1252, 2023.
doi: 10.3390/molecules28031252
[29] Lin RD, Chin YP, Hou WC, Lee MH. The Effects of Antibiotics Combined with Natural Polyphenols against Clinical Methicillin-Resistant Staphylococcus aureus (MRSA), Planta Medica, 74(8): 840–846, 2008.
doi: 10.1055/s-2008-1074559
[30] Duda-Madej A, Stecko J, Sobieraj J, Szymańska N, Kozłowska J. Naringenin and Its Derivatives—Health-Promoting Phytobiotic against Resistant Bacteria and Fungi in Humans, Antibiotics, 11(11): 1628, 2022.
doi: 10.3390/antibiotics11111628
[31] Ming D,Wang D, Cao F, Xiang H, Mu D, Cao J, Li B, Zhong L, Dong X, Zhong X,Wang L,Wang T. Kaempferol Inhibits the Primary Attachment Phase of Biofilm Formation in Staphylococcus aureus, Frontiers in Microbiology, 8: 2263, 2017.
doi: 10.3389/fmicb.2017.02263
[32] Alves MJ, Ferreira ICFR, Froufe HJC, Abreu RMV, Martins A, Pintado M. Antimicrobial activity of phenolic compounds identified in wild mushrooms, SAR analysis and docking studies, Journal of Applied Microbiology, 115(2): 346–357, 2013.
doi: 10.1111/jam.12196
[33] Morimoto Y, Baba T, Sasaki T, Hiramatsu K. Apigenin as an anti-quinolone-resistance antibiotic, International Journal of Antimicrobial Agents, 46(6): 666–673, 2015.
doi: 10.1016/j.ijantimicag.2015.09.006
doi: 10.1016/j.foodchem.2018.05.055
[2] Chirinos R, Necochea O, Pedreschi R, Campos D. Sacha inchi (Plukenetia volubilis L.) shell: An alternative source of phenolic compounds and antioxidants, International Journal of Food Science and Technology, 51(4): 986–993, 2016.
doi: 10.1111/ijfs.13049
[3] Sanchez-Reinoso Z, Mora-Adames WI, Fuenmayor CA, Darghan-Contreras AE, Gardana C, Gutiérrez LF. Microwave-assisted extraction of phenolic compounds from Sacha Inchi shell: Optimization, physicochemical properties and evaluation of their antioxidant activity, Chemical Engineering and Processing: Process Intensification, 153: 107922, 2020.
doi: 10.1016/j.cep.2020.107922
[4] Sainakham M, Mungmai L. In vitro anti-oxidative activity and tyrosinase inhibition of inca peanut (Plukenetia volubilis L.) shell extracts from different preparation methods, Thai Journal of Science and Technology (TJST), 9(3): 407–417, 2020.
doi: 10.14456/tjst.2020.30
[5] Li P, Cai X, Xiao N, Ma X, Zeng L, Zhang LH, Xie L, Du B. Sacha inchi (Plukenetia volubilis L.) shell extract alleviates hypertension in association with the regulation of gut microbiota, Food & Function, 11(9): 8051–8067, 2020.
doi: 10.1039/D0FO01770A
[6] Prasongsub W, Pimsan N, Buranapattarachote C, Punturee K. Anti-HMG-CoA reductase and antioxidant activities of Sacha inchi (Plukenetia volubilis L.) nutshell extract, Journal of Associated Medical Sciences, 54(3): 18–26, 2021.
doi: 10.14456/jams.2021.19
[7] Thuanthong A, Klomklao S, Panyo J, Zhang Y. In-Vitro Screenings for Biological and Antioxidant Activities of Aqueous Extract from Sacha Inchi (Plukenetia volubilis L.) Husks, Trends in Sciences, 20(11): 6815, 2023.
doi: 10.48048/tis.2023.6815
[8] Kittibunchakul S, Hudthagosol C, Sanporkha P, Sapwarobol S, Temviriyanukul P, Suttisansanee U. Evaluation of Sacha Inchi (Plukenetia volubilis L.) By-Products as Valuable and Sustainable Sources of Health Benefits, Horticulturae, 8(4): 344, 2022.
doi: 10.3390/horticulturae8040344
[9] Gonzalez-Aspajo G, Belkhelfa H, Haddioui-Hbabi L, Bourdy G, Deharo E. Sacha Inchi Oil (Plukenetia volubilis L.), effect on adherence of Staphylococus aureus to human skin explant and keratinocytes in vitro, Journal of Ethnopharmacology, 171: 330–334, 2015.
doi: 10.1016/j.jep.2015.06.009
[10] Wintachai P, Voravuthikunchai SP. Characterization of Novel Lytic Myoviridae Phage Infecting Multidrug-Resistant Acinetobacter baumannii and Synergistic Antimicrobial Efficacy between Phage and Sacha Inchi Oil, Pharmaceuticals, 15(3): 291, 2022.
doi: 10.3390/ph15030291
[11] Ampofo J, Ngadi M. Ultrasound-assisted processing: Science, technology and challenges for the plant-based protein industry, Ultrasonics Sonochemistry, 84: 105955, 2022.
doi: 10.1016/j.ultsonch.2022.105955
[12] Dastmalchi K, Damien-Dorman HJ, Koşar M, Hiltunen R. Chemical composition and in vitro antioxidant evaluation of a water-soluble Moldavian balm (Dracocephalum moldavica L.) extract, LWT, 40(2): 239–248, 2007.
doi: 10.1016/j.lwt.2005.09.019
[13] Ou B, Hampsch-Woodill M, Prior RL. Development and Validation of an Improved Oxygen Radical Absorbance Capacity Assay Using Fluorescein as the Fluorescent Probe, Journal of Agricultural and Food Chemistry, 49(10): 4619–4626, 2001.
doi: 10.1021/jf010586o
[14] Huang D, Ou B, Hampsch-Woodill M, Flanagan JA, Deemer EK. Development and Validation of Oxygen Radical Absorbance Capacity Assay for Lipophilic Antioxidants Using Randomly Methylated B-Cyclodextrin as the Solubility Enhancer, Journal of Agricultural and Food Chemistry, 50(7): 1815–1821, 2002.
doi: 10.1021/jf0113732
[15] CLSI. Performance standards for antimicrobial disk susceptibility tests: Approved standard, Clinical and Laboratory Standards Institute, 2012.
https://clsi.org/media/1631/m02a12_sample.pdf
[16] Zahari NAAR, Chong GH, Abdullah LC, Chua BL. Ultrasonic-Assisted Extraction (UAE) Process on Thymol Concentration from Plectranthus Amboinicus Leaves: Kinetic Modeling and Optimization, Processes, 8(3): 322, 2020.
doi: 10.3390/pr8030322
[17] Hernández-Rodríguez P, Baquero LP, Larrota HR. Flavonoids: Potential Therapeutic Agents by Their Antioxidant Capacity, Bioactive Compounds: Health Benefits and Potential Applications; p. 265–288, 2018.
doi: 10.1016/B978-0-12-814774-0.00014-1
[18] Arias A, Feijoo G, Moreira MT. Exploring the potential of antioxidants from fruits and vegetables and strategies for their recovery, Innovative Food Science and Emerging Technologies, 77: 102974, 2022.
doi: 10.1016/j.ifset.2022.102974
[19] Santos-Sánchez NF, Salas-Coronado R, Villanueva-Cañongo C, Hernández-Carlos B. Antioxidant Compounds and Their Antioxidant Mechanism, Antioxidants. IntechOpen, 2019.
doi:10.5772/intechopen.85270
[20] Rakha A, Umar N, Rabail R, Butt MS, Kieliszek M, Hassoun A, Aadil RM. Anti-inflammatory and anti-allergic potential of dietary flavonoids: A review, Biomedicine & Pharmacotherapy, 156: 113945, 2022.
doi: 10.1016/j.biopha.2022.113945
[21] Zeb A. Concept, mechanism, and applications of phenolic antioxidants in foods, Journal of Food Biochemistry, 44(9): 1–22, 2020.
doi: 10.1111/jfbc.13394
[22] Khan A, Heng W, Wang Y, Qiu J, Wei X, Peng S, Saleem S, Khan M, Ali SS, Wei DQ. In silico and in vitro evaluation of kaempferol as a potential inhibitor of the SARS-CoV -2 main protease
(3CLpro), Phytotherapy Research, 35(6): 2841–2845, 2021.
doi: 10.1002/ptr.6998
[23] Tutunchi H, Naeini F, Ostadrahimi A, Hosseinzadeh-Attar MJ. Naringenin, a flavanone with antiviral and anti-inflammatory effects: A promising treatment strategy against COVID-19, Phytotherapy Research, 34(12): 3137–3147, 2020.
doi: 10.1002/ptr.6781
[24] Nascimento AKL, Melo-Silveira RF, Dantas-Santos N, Fernandes JM, Zucolotto SM, Rocha HAO, Scortecci KC. Antioxidant and Antiproliferative Activities of Leaf Extracts from Plukenetia volubilis Linneo (Euphorbiaceae), Evidence-Based Complementary and Alternative Medicine, 2013: 950272, 2013.
doi: 10.1155/2013/950272
[25] Vaou N, Stavropoulou E, Voidarou C, Tsigalou C, Bezirtzoglou E. Towards Advances in Medicinal Plant Antimicrobial Activity: A Review Study on Challenges and Future Perspectives, Microorganisms, 9(10): 2041, 2021.
doi: 10.3390/microorganisms9102041
[26] Adekola HA, Adeleye AO, Adesetan TO, Folorunso JB, Odeyemi FA. Antibacterial Activity of Vanillic Acid against Staphylococcus aureus, Salmonella typhi, and Proteus mirabilis, Microbes, Infection & Chemotherapy, 2(12): e1458, 2022.
doi: 10.54034/mic.e1548
[27] Resende FA, Nogueira LG, Bauab TM, Vilegas W, Varanda EA. Antibacterial potential of flavonoids with different hydroxylation patterns, Eclética Química Journal, 40(1): 173, 2015.
doi: 10.26850/1678-4618eqj.v40.1.2015.p173-179
[28] Veiko AG, Olchowik-Grabarek E, Sekowski S, Roszkowska A, Lapshina EA, Dobrzynska I, Zamaraeva M, Zavodnik IB. Antimicrobial Activity of Quercetin, Naringenin and Catechin: Flavonoids Inhibit Staphylococcus aureus-Induced Hemolysis and Modify Membranes of Bacteria and Erythrocytes, Molecules, 28(3): 1252, 2023.
doi: 10.3390/molecules28031252
[29] Lin RD, Chin YP, Hou WC, Lee MH. The Effects of Antibiotics Combined with Natural Polyphenols against Clinical Methicillin-Resistant Staphylococcus aureus (MRSA), Planta Medica, 74(8): 840–846, 2008.
doi: 10.1055/s-2008-1074559
[30] Duda-Madej A, Stecko J, Sobieraj J, Szymańska N, Kozłowska J. Naringenin and Its Derivatives—Health-Promoting Phytobiotic against Resistant Bacteria and Fungi in Humans, Antibiotics, 11(11): 1628, 2022.
doi: 10.3390/antibiotics11111628
[31] Ming D,Wang D, Cao F, Xiang H, Mu D, Cao J, Li B, Zhong L, Dong X, Zhong X,Wang L,Wang T. Kaempferol Inhibits the Primary Attachment Phase of Biofilm Formation in Staphylococcus aureus, Frontiers in Microbiology, 8: 2263, 2017.
doi: 10.3389/fmicb.2017.02263
[32] Alves MJ, Ferreira ICFR, Froufe HJC, Abreu RMV, Martins A, Pintado M. Antimicrobial activity of phenolic compounds identified in wild mushrooms, SAR analysis and docking studies, Journal of Applied Microbiology, 115(2): 346–357, 2013.
doi: 10.1111/jam.12196
[33] Morimoto Y, Baba T, Sasaki T, Hiramatsu K. Apigenin as an anti-quinolone-resistance antibiotic, International Journal of Antimicrobial Agents, 46(6): 666–673, 2015.
doi: 10.1016/j.ijantimicag.2015.09.006
How to Cite
Polanía Cuellar, N. V., Hernández Peñaranda, I. P., Villalba Rey, D., Acuña Rodríguez, K. N., & Gómez Jaimes, F. N. (2024). Sacha inchi (Plukenetia volubilis L.) husks and seed shells are sources of phenolic compounds with potential health benefits. Universitas Scientiarum, 29(3), 275–291. https://doi.org/10.11144/Javeriana.SC293.siha
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