Abstract
Cladodes from Opuntia ficus indica var. Atlixco serve as a valuable source of dietary fiber and bioactive compounds. This study delves into the chemical composition, total polyphenolic content, and antioxidant capacity of powdered samples at three ripening stages. Notably, cladodes at 60 days of ripening (60 d) exhibited the highest dietary fiber content, while those at 45 days of ripening (45 d) showcased superior levels of total polyphenols and antioxidant capacity, as measured by ABTS. Key minerals identified through ICP-OES included Ca, K, Mg, P, and Na, with Ca and K being more abundant. Liquid chromatography–electrospray ionization–tandem mass spectrometry (LC-ESI-MS/MS) facilitated the identification and quantification of polyphenols in 60 d cladodes. Despite their size (> 30 cm), rendering them unsuitable for commercialization, these cladodes’ extract revealed elevated proportions of piscidic and eucomic acids, along with isorhamnetin derivatives. Evaluation of oxidative stress resistance and anti-adipogenic capacity in a Caenorhabditis elegans animal model revealed that the extract from 60 d cladodes enhanced the survival rate under oxidative stress conditions and reduced fat deposition in the C. elegans intestine. These findings not only highlight the health and nutritional advantages but also inspire further research and the potential development of innovative functional products.
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References
del M. Socorro Santos Díaz, B. de la Rosa, A.-P. Héliès-Toussaint, C. Guéraud, F. Nègre-Salvayre, A., Opuntia spp.: Characterization and Benefits in Chronic Diseases. Oxid. Med. Cell. Longev., 1–17 (2017). https://doi.org/10.1155/2017/8634249
M. Bautista-Justo, R.I. Pineda Torres, E. Camarena-Aguilar, G. Alanís- Guzmán, Da V.M. Mota, J.E. Barboza- Corona, El Nopal fresco como fuente de fibra y calcio en panqués. Acta Univ. 20, 11–17 (2010). https://doi.org/10.15174/au.2010.62
M.I. Hernández-Urbiola, E. Pérez-Torrero, M.E. Rodríguez-García, Chemical Analysis of Nutritional Content of Prickly pads (Opuntia ficus indica) at Varied ages in an Organic Harvest. Int. J. Environ. Res. Public. Health. 8, 1287–1295 (2011). https://doi.org/10.3390/ijerph8051287
M.G. Astello-García, I. Cervantes, V. Nair, M. Santos-Díaz del, S. Reyes-Agüero, A. Guéraud, F. Negre-Salvayre, A. Rossignol, M. Cisneros-Zevallos, L. de la Rosa, A.P., Chemical composition and phenolic compounds profile of cladodes from Opuntia spp. cultivars with different domestication gradient. J. Food Compos. Anal. 43, 119–130 (2015). https://doi.org/10.1016/j.jfca.2015.04.016
C.E. Aruwa, S.O. Amoo, T. Kudanga, Opuntia (Cactaceae) plant compounds, biological activities and prospects – A comprehensive review. Food Res. Int. 112, 328–344 (2018). https://doi.org/10.1016/j.foodres.2018.06.047
R. Ciriminna, N. Chavarría-Hernández, A.I. Rodríguez‐Hernández, M. Pagliaro, Toward unfolding the bioeconomy of nopal (Opuntia spp). Biofuels Bioprod. Biorefining. 13, 1417–1427 (2019). https://doi.org/10.1002/bbb.2018
M. Quintero-García, E. Gutiérrez-Cortez, M. Bah, A. Rojas-Molina, M. Cornejo-Villegas, A. de los, Del A. Real, I. Rojas-Molina, Comparative analysis of the Chemical Composition and Physicochemical properties of the mucilage extracted from Fresh and dehydrated Opuntia ficus indica Cladodes. Foods. 10, 2137 (2021). https://doi.org/10.3390/foods10092137
K. El-Mostafa, E. Kharrassi, Y. Badreddine, A. Andreoletti, P. Vamecq, J.E. Kebbaj, M. Latruffe, N. Lizard, G. Nasser, B. Cherkaoui-Malki, Nopal Cactus (Opuntia ficus-indica) as a source of Bioactive Compounds for Nutrition, Health and Disease. Molecules. 19, 14879–14901 (2014). https://doi.org/10.3390/molecules190914879
P.I. Angulo-Bejarano, O. Martínez-Cruz, O. Paredes-Lopez, P. Content, Nutraceutical potential and biotechnological applications of an ancient Mexican plant: Nopal (Opuntia ficus-indica). Curr. Nutr. Food Sci. 10, 196–217 (2014). https://doi.org/10.2174/157340131003140828121015
A.K.B. Corsi, M. Chalfie, A tranparent window into biology: a primer on caenorhabditis elegans. Genetics. 200, 387–407 (2015)
S. Brenner, The genetics of Caenorhabditis elegans. Genetics. 77, 71–94 (1974)
W. Chen, L. Rezaizadehnajafi, M. Wink, Influence of resveratrol on oxidative stress resistance and life span in Caenorhabditis elegans. J. Pharm. Pharmacol. 65, 682–688 (2013)
N. Mudd, A.M. Liceaga, Caenorhabditis elegans as an in vivo model for food bioactives: a review. Curr. Res. Food Sci. 5, 845–856 (2022). https://doi.org/10.1016/j.crfs.2022.05.001
A.O.A.C. 2000. Official Methods of Analysis Association of Official Analytical Chemist. EUA
L. Prosky, de L. Vries, S. Lee, Determination of total, soluble and insoluble dietary fiber in foods; enzymatic-gravimetric method: collaborative study. J. AOAC Int. 73, 395–416 (1992)
De E. Santiago, G. Pereira-Caro, J.M. Moreno-Rojas, C. Cid, De M.-P. Peña, Digestibility of (poly)phenols and antioxidant activity in raw and cooked Cactus Cladodes (Opuntia ficus-indica). J. Agric. Food Chem. 66, 5832–5844 (2018). https://doi.org/10.1021/acs.jafc.8b01167
K.I. Ereifej, H. Feng, T.M. Rababah, S.H. Tashtoush, M.H. Al-U’datt, S. Gammoh, G.J. Al-Rabadi, Effect of Extractant and temperature on Phenolic compounds and antioxidant activity of selected spices. Food Nutr. Sci. 07, 362–370 (2016). https://doi.org/10.4236/fns.2016.75038
W. Brand-Williams, M. Cuvelier, C. Berset, Use of Free Radical Method to evaluate antioxidant activity. LWT-Food Sci. Technol. 28, 25–30 (1995)
R. Re, N. Pellegrini, A. Proteggente, A. Pannala, M. Yang, C. Rice-Evans, Antioxidant activity applying an Improved ABTS Radical Cation Decolorization Assay. Free Radical Biol. Med. 26, 1231–1237 (1999)
T. Stiernagle, Maintenance of C. elegans. WormBook. (2006)
F. Surco-Laoos, J. Cabello, E. Gomez-Orte, S. Gonzales-Manzano, A. Gonzalez_Paramas, C. Santos-Buelga, M. Dueñas, Effects of O-methylated metabolites of quercetin on oxidative stress, thermotolerance, lifespan and bioavailability on Caenohabditis Elegans. Food Funct. 2, 445 (2011)
J.S. Sangha, D. Fan, A.H. Banskota, R. Stefanova, W. Khan, J. Hafting, J. Craigie, A.T. Critchley, B. Prithiviraj, Bioactive components of the edible strain of red alga, Chondrus crispus, enhance oxidative stress tolerance in Caenorhabditis elegans. J. Funct. Foods. 5, 1180–1190 (2013). https://doi.org/10.1016/j.jff.2013.04.001
S. Sugawara, T. Honma, J. Ito, R. Kijima, T. Tsuduki, Fish oil changes the lifespan of Caenorhabditis elegans via lipid peroxidation. J. Clin. Biochem. Nutr. 52, 139–145 (2013)
W. Escorcia, D.L. Ruter, J. Nhan, S.P. Curran, Quantification of lipid abundance and evaluation of lipid distribution in Caenorhabditis elegans by Nile Red and Oil Red O staining. J. Vis. Exp. 57352 (2018). https://doi.org/10.3791/57352
M.E. Rodríguez-Garcia, de C. Lira, E. Hernández-Becerra, M.A. Cornejo-Villegas, A.J. Palacios-Fonseca, I. Rojas-Molina, R. Reynoso, L.C. Quintero, A. Del-Real, T.A. Zepeda, C. Muñoz-Torres, Physicochemical Characterization of Nopal Pads (Opuntia ficus indica) and dry Vacuum Nopal powders as a function of the maturation. Plant. Foods Hum. Nutr. 62, 107–112 (2007). https://doi.org/10.1007/s11130-007-0049-5
S. Bensadón, D. Hervert-Hernández, S.G. Sáyago-Ayerdi, I. Goñi, By-Products of Opuntia ficus-indica as a source of antioxidant Dietary Fiber. Plant. Foods Hum. Nutr. 65, 210–216 (2010). https://doi.org/10.1007/s11130-010-0176-2
M. Dick, C. Limberger, C. Silveira Thys, R. de Oliveira Rios, A. Hickmann, S. Flôres, Mucilage and cladode flour from cactus (Opuntia monacantha) as alternative ingredients in gluten-free crackers. Food Chem. 314, 126178 (2020). https://doi.org/10.1016/j.foodchem.2020.126178
M. Aguilera-Barreiro, de los A. Rivera-Márquez, J.A. Trujillo-Arriaga, H.M. Tamayo y Orozco, J.A. Barreira-Mercado, E. Rodríguez-García, Intake of dehydrated nopal (Opuntia ficus indica) improves bone mineral density and calciuria in adult Mexican women. Food Nutr. Res. 57, 19106 (2013). https://doi.org/10.3402/fnr.v57i0.19106
B. Nabil, R. Ouaabou, M. Ouhammou, L. Saadouni, M. Mahrouz, Impact of particle size on functional, physicochemical properties and antioxidant activity of cladode powder (Opuntia ficus-indica). J. Food Sci. Technol. 57, 943–954 (2020). https://doi.org/10.1007/s13197-019-04127-4
C. Anchondo-Trejo, J.A. Loya-Carrasco, T. Galicia-García, I. Estrada-Moreno, M. Mendoza-Duarte, L. Castellanos-Gallo, R. Márquez-Meléndez, B. Portillo-Arroyo, C. Soto-Figueroa, Development of a third generation snack of Rice Starch enriched with Nopal Flour (Opuntia ficus indica). Molecules. 26, 54 (2020). https://doi.org/10.3390/molecules26010054
M. Missaoui, I. D’Antuono, M. D’Imperio, V. Linsalata, S. Boukhchina, A.F. Logrieco, A. Cardinali, Characterization of micronutrients, Bioaccessibility and antioxidant activity of Prickly Pear Cladodes as functional ingredient. Molecules. 25, 2176 (2020). https://doi.org/10.3390/molecules25092176
E. Ramírez-Moreno, C.D. Marqués, M.C. Sánchez-Mata, I. Goñi, In vitro calcium bioaccessibility in raw and cooked cladodes of prickly pear cactus (Opuntia ficus-indica L. Miller). LWT - Food Sci. Technol. 44, 1611–1615 (2011). https://doi.org/10.1016/j.lwt.2011.01.001
F. Blando, R. Russo, C. Negro, De L. Bellis, S. Frassinetti, Antimicrobial and Antibiofilm Activity against Staphylococcus aureus of Opuntia ficus-indica (L.) Mill. Cladode Polyphenolic Extracts Antioxid. 8, 117 (2019). https://doi.org/10.3390/antiox8050117
L. Santos-Zea, J.A. Gutiérrez-Uribe, S.O. Serna-Saldivar, Comparative Analyses of Total Phenols, antioxidant activity, and Flavonol Glycoside Profile of Cladode flours from different varieties of Opuntia spp. J. Agric. Food Chem. 59, 7054–7061 (2011). https://doi.org/10.1021/jf200944y
S.S. El-Hawary, M. Sobeh, W.K. Badr, M.A.O. Abdelfattah, Z.Y. Ali, M.E. El-Tantawy, M.A. Rabeh, M. Wink, HPLC-PDA-MS/MS profiling of secondary metabolites from Opuntia ficus-indica cladode, peel and fruit pulp extracts and their antioxidant, neuroprotective effect in rats with aluminum chloride induced neurotoxicity. Saudi J. Biol. Sci. 27, 2829–2838 (2020). https://doi.org/10.1016/j.sjbs.2020.07.003
A. Ressaissi, N. Attia, P.L. Falé, R. Pacheco, B.L. Victor, M. Machuqueiro, M.L.M. Serralheiro, Isorhamnetin derivatives and piscidic acid for hypercholesterolemia: cholesterol permeability, HMG-CoA reductase inhibition, and docking studies. Arch. Pharm. Res. 40, 1278–1286 (2017). https://doi.org/10.1007/s12272-017-0959-1
J. Zhang, X. Xue, Y. Yang, W. Ma, Y. Han, X. Qin, Multiple biological defects caused by calycosin-7-O-β-d-glucoside in the nematode Caenorhabditis elegans are associated with the activation of oxidative damage. J. Appl. Toxicol. 38, 801–809 (2018)
C. Moliner, L. Barros, M. Dias, V. López, E. Langa, I. Ferreira, C. Gómez-Rincón, Edible flowers of Tagetes erecta L. as Functional ingredients: phenolic composition, antioxidant and Protective effects on Caenorhabditis elegans. Nutrients. 10, 2002 (2018). https://doi.org/10.3390/nu10122002
J. Zheng, F. Enright, M. Keenan, J. Finley, J. Zhou, J. Ye, F. Greenway, R.N. Senevirathne, C.R. Gissendanner, R. Manaois, A. Prudente, J.M. King, R. Martin, R. Starch, Fermented resistant starch, and short-chain fatty acids reduce intestinal Fat Deposition in Caenorhabditis elegans. J. Agric. Food Chem. 58, 4744–4748 (2010). https://doi.org/10.1021/jf904583b
C. Gao, Z. Gao, F.L. Greenway, J.H. Burton, W.D. Johnson, M.J. Keenan, F.M. Enright, R.J. Martin, Y. Chu, J. Zheng, Oat consumption reduced intestinal fat deposition and improved health span in Caenorhabditis elegans model. Nutr. Res. 35, 834–843 (2015). https://doi.org/10.1016/j.nutres.2015.06.007
C.F. Rodrigues, W. Salgueiro, M. Bianchini, J.C. Veit, R.L. Puntel, T. Emanuelli, C.C. Dernadin, D.S. Ávila, Salvia hispanica L. (Chia) seeds oil extracts reduce lipid accumulation and produce stress resistance in Caenorhabditis elegans. Nutr. Metab. 15, 83 (2018). https://doi.org/10.1186/s12986-018-0317-4
Y. Yue, S. Li, P. Shen, Y. Park, Caenorhabditis elegans as a model for obesity research. Curr. Res. Food Sci. 4, 692–697 (2021). https://doi.org/10.1016/j.crfs.2021.09.008
Acknowledgements
R.A.O. acknowledge to Universidad de las Américas Puebla (UDLAP) and Consejo Nacional de Humanidades, Ciencias y Tecnología (CONAHCYT) for the scholarship granted to complete her doctoral degree. The authors thank Food Analysis Laboratory Intema S.A. de C.V. for its contribution in mineral and polyphenol profile analysis in Opuntia ficus indica.
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Conceptualization, R.A.O., J.D.L.R., M.M.R.R., and A.E.O.R; methodology, R.A.O., J.D.L.R., M.M.R.R., and A.E.O.R; validation, T.S.P., K.V.L., M.M.R.R., and A.E.O.R; formal analysis, J.D.L.R., C.A.P., T.S.P., K.V.L. M.M.R.R., and A.E.O.R; investigation, R.A.O., J.D.L.R., M.M.R.R., and A.E.O.R; resources, M.M.R.R., C.A.P., and A.E.O.R.; data curation, R.A.O. and T.S.P.; writing—original draft preparation, R.A.O., J.D.L.R., M.M.R.R., and A.E.O.R; writing—review and editing, R.A.O., J.D.L.R., M.M.R.R., and A.E.O.R; visualization, R.A.O. and J.D.L.R.; supervision, J.D.L.R., M.M.R.R, and A.E.O.R.; project administration, A.E.O.R.; funding acquisition, C.A.P, M.M.R.R., and A.E.O.R.
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Aparicio-Ortuño, R., Lozada-Ramírez, J.D., de Parrodi, C.A. et al. Characterization of mexican Opuntia ficus indica cladode and bioactive compound profile. Oxidative stress resistance and anti-adipogenic effect in Caenorhabditis elegans. Food Measure (2024). https://doi.org/10.1007/s11694-024-02602-x
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DOI: https://doi.org/10.1007/s11694-024-02602-x