Abstract
In the present work, Calabrian apple juices belonging to four different cultivars, Royal Gala, Pink Lady, Golden Delicious, and Fuji, were studied. One of the objectives of this work was the characterization of metabolites present in the food matrix and at the same time the possibility of using innovative methodologies based on membrane operations, such as ultrafiltration (UF) and nanofiltration (NF), to obtain from the squeezed apple juice, extracts rich in antioxidants. To improve the overall quality of the study and enhance the coverage of the metabolome two analytical tools were used: NMR and HPLC–UV-ESI–MS/MS. One- and two-dimensional multinuclear NMR spectra combined with chemometric analysis (PCA) were used to identify the metabolic profile of different juice varieties and variations in metabolic composition. On the basis of its higher content of phenolic compounds, the Golden Delicious variety was selected to carry out membrane filtration tests. Specifically, the fresh juice was clarified by UF and then concentrated by NF up to a volume reduction factor (VRF) of 3.3. Permeate and retentate fractions of both processes were analyzed by HPLC–UV and NMR in order to evaluate the membrane selectivity of the selected membranes towards target compounds.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Abreu, A. C., & Fernández, I. (2020). NMR metabolomics applied on the discrimination of variables influencing tomato (Solanum lycopersicum). Molecules, 25(16), 3738. https://doi.org/10.3390/molecules25163738
Arend, G. D., Rezzadori, K., Soares, L. S., & Petrus, J. C. C. (2019). Performance of nanofiltration process during concentration of strawberry juice. Journal of Food Science & Technology-Mysore, 56(4), 2312–2319. https://doi.org/10.1007/s13197-019-03659-z
Azmir, J., Zaidul, I. S. M., Rahman, M. M., Sharif, K. M., Mohamed, A., Sahena, F., Jahurul, M. H. A., Ghafoor, K., Norulain, N. A. N., & Omar, A. K. M. (2013). Techniques for extraction of bioactive compounds from plant materials: A review. Journal of Food Engineering, 117(4), 426–436. https://doi.org/10.1016/j.jfoodeng.2013.01.014
Belton, P. S., Delgadillo, I., Gil, A. M., Roma, P., Casuscelli, F., Colquhoun, I. J., et al. (1997). High-field proton studies of apple juices. Magnetic Resonance in Chemistry, 35, S52–S60.
Bhattacharjee, C., Saxena, V. K., & Dutta, S. (2017). Fruit juice processing using membrane technology: A review. Innovative Food Science and Emerging Technologies, 43, 136–153. https://doi.org/10.1016/j.ifset.2017.08.002
Bingol, K. (2018). Recent advances in targeted and untargeted metabolomics by NMR and MS/NMR methods. High-Throughput, 7, 9. https://doi.org/10.3390/ht7020009
Boyer, J., & Liu, R. H. (2004). Apple phytochemicals and their health benefits. Nutrition Journal, 3, 1–15. https://doi.org/10.1186/1475-2891-3-5
Borgognone, M. G., Bussi, J., & Hough, G. (2001). Principal component analysis in sensory analysis: Covariance or correlation matrix? Food Quality and Preference, 12, 323–326. https://doi.org/10.1016/S0950-3293(01)00017-9.
Brans, G., Schroën, C. G. P. H., Van der Sman, R. G. M., & Boom, R. M. (2004). Membrane fractionation of milk: State of the art and challenges. Journal of Membrane Science, 243, 263–272. https://doi.org/10.1016/j.memsci.2004.06.029
Cai, M., Hou, W. Z., Lv, Y. Q., & Sun, P. L. (2017). Behavior and rejection mechanisms of fruit juice phenolic compounds in model solution during nanofiltration. Journal of Food Engineering, 195, 97–104. https://doi.org/10.1007/s11947-017-1970-8
Cassano, A., Cabri, W., Mombelli, G., Peterlongo, F., & Giorno, L. (2016). Recovery of bioactive compounds from artichoke brines by nanofiltration. Food and Bioproducts Processing, 98, 257–265. https://doi.org/10.1016/j.fbp.2016.02.004
Castro-Muñoz, R., Yáñez-Fernández, J., & Fíla, V. (2016). Phenolic compounds recovered from agro-food by-products using membrane technologies: An overview. Food Chemistry, 213, 753–762. https://doi.org/10.1016/j.foodchem.2016.07.030
Castro-Muñoz, R., Conidi, C., & Cassano, A. (2018). Membrane-based technologies for meeting the recovery of biologically active compounds from foods and their by-products. Critical Reviews in Food Science and Nutrition, 59(18), 2927–2948. https://doi.org/10.1080/10408398.2018.1478796
Catarino, M., & Mendes, A. (2011). Dealcoholizing wine by membrane separation processes. Innovative Food Science & Emerging Technologies, 12(3), 330–337. https://doi.org/10.1016/j.ifset.2011.03.006
Conidi, C., Cassano, A., & Drioli, E. (2011). A membrane-based study for the recovery of polyphenols from bergamot juice. Journal of Membrane Science, 375(1–2), 182–190. https://doi.org/10.1016/j.memsci.2011.03.035
Conidi, C., & Cassano, A. (2014). Recovery of phenolic compounds from bergamot juice by nanofiltration membranes. Desalination and Water Treatment, 56(13), 3510–3518. https://doi.org/10.1080/19443994.2014.968219
Conidi, C., Fucà, L., Drioli, E., & Cassano, A. (2019). A membrane-based process for the recovery of glycyrrhizin and phenolic compounds from licorice wastewaters. Molecules, 24, 2279. https://doi.org/10.3390/molecules24122279
Cuthbertson, D., Andrews, P. K., Reganold, J. P., Davies, N. M., & Lange, B. M. (2012). Utility of metabolomics toward assessing the metabolic basis of quality traits in apple fruit with an emphasis on antioxidants. Journal of Agricultural and Food Chemistry, 60(35), 8552–8560. https://doi.org/10.1021/jf3031088
Duda-Chodak, A., Tarko, T., Satora, P., Sroka, P., & Tuszyńsk, T. (2010). The profile of polyphenols and antioxidant properties of selected apple cultivars grown in Poland. Journal of Fruit and Ornamental Plant Research, 18(2), 39–50.
Ebrahimi, P., Viereck, N., Bro, R., & Engelsen, S. B. (2017). Chemometric analysis of NMR spectra. In A. G. Webb (Ed.), Modern Magnetic Resonance (pp. 1649–1668). Springer.
Eisenmann, P., Ehlers, M., Weinert, C. H., Tzvetkova, P., Silber, M., Rist, M. J., Rist, M. J., Luy, B., & Muhle-Goll, C. (2016). Untargeted NMR spectroscopic analysis of the metabolic variety of new apple cultivars. Metabolites, 6(3), 29. https://doi.org/10.3390/metabo6030029
Figoli, A., Tagarelli, A., Mecchia, A., Trotta, A., Cavaliere, B., Lavecchia, R., Sindona, G., & Drioli, E. (2006). Enzyme-assisted pervaporative recovery of concentrated bergamot peel oils. Desalination, 199(1–3), 111–112. https://doi.org/10.1016/j.desal.2006.03.025
Francini, A., & Sebastiani, L. (2013). Phenolic compounds in apple (Malus × domestica Borkh.): Compounds characterization and stability during postharvest and after processing. Antioxidants, 2(3), 181–193. https://doi.org/10.3390/antiox2030181
Francini, A., Romeo, S., Cifelli, M., Gori, D., Domenici, V., & Sebastiani, L. (2017). 1H NMR and PCA-based analysis revealed variety dependent changes in phenolic contents of apple fruit after drying. Food Chemistry, 221, 1206–1213. https://doi.org/10.1016/j.foodchem.2016.11.038
Galaverna, G., Di Silvestro, G., Cassano, A., Sforza, S., Dossena, A., Drioli, E., & Marchelli, R. (2008). A new integrated membrane process for the production of concentrated blood orange juice: Effect on bioactive compounds and antioxidant activity. Food Chemistry, 106(3), 1021–1030. https://doi.org/10.1016/j.foodchem.2007.07.018
Garcia-Castello, E. M., Mayor, L., Chorques, S., Arguelles, A., Vidal-Brotons, D., & Gras, M. L. (2011). Reverse osmosis concentration of press liquor from orange juice solid wastes: Flux decline mechanisms. Journal of Food Engineering, 106(3), 199–205. https://doi.org/10.1016/j.jfoodeng.2011.05.005
Gathungu, R. M., Kautz, R., Kristal, B. S., Bird, S. S., & Vouros, P. (2018). The integration of LC-MS and NMR for the analysis of low molecular weight trace analytes in complex matrices. Mass Spectrometry Reviews, 39, 35–54. https://doi.org/10.1002/mas.21575
Gerhauser, C. (2008). Cancer chemopreventive potential of apples, apple juice, and apple components. Planta Medica, 74(13), 1608–1624. https://doi.org/10.1055/s-0028-1088300
Gören, A. C., Çıkrıkçı, S., Çergel, M., & Bilsel, G. (2009). Rapid quantitation of curcumin in turmeric via NMR and LC–tandem mass spectrometry. Food Chemistry, 113(4), 1239–1242. https://doi.org/10.1016/j.foodchem.2008.08.014
Gunathilake, C., & Considine, M. (2018). Flavonoids rich apple for healthy life. MOJ Food Processing & Technology, 6(1), 89–91. https://doi.org/10.15406/mojfpt.2018.06.00149
Harker, F. R., Gunson, F. A., & Jaeger, S. R. (2003). The case for fruit quality: An interpretive review of consumer attitudes, and preferences for apples. Postharvest Biology and Technology, 28(3), 333–347. https://doi.org/10.1016/S0925-5214(02)00215-6
Iaccarino, N., Varming, C., Petersen, M. A., Viereck, N., Schütz, B., Toldam-Andersen, T. B., Randazzo, A., & Engelsen, S. B. (2019). Ancient Danish apple cultivars — A comprehensive metabolite and sensory profiling of apple juices. Metabolites, 9(7), 139. https://doi.org/10.3390/metabo9070139.
Jeong, S. W., Kim, G.-S., Lee, W. S., Kim, Y.-H., Kang, N. J., Jin, J. S., Lee, G. M., Kim, S. T., El-Aty, A. M. A., Shim, J.-H., & Shin, S. C. (2015). The effects of different night-time temperatures and cultivation durations on the polyphenolic contents of lettuce: Application of principal component analysis. Journal of Advanced Research, 6(3), 493–499. https://doi.org/10.1016/j.jare.2015.01.004
Kahle, K., Kraus, M., & Richling, E. (2005). Polyphenol profiles of apple juices. Molecular Nutrition & Food Research, 49, 797–806. https://doi.org/10.1002/mnfr.200500064
Koutsos, A., Tuohy, K. M., & Lovegrove, J. A. (2015). Apples and cardiovascular health—Is the gut microbiota a core consideration? Nutrients, 7(6), 3959–3998. https://doi.org/10.3390/nu7063959
Kumar, S., Bink, M. C. A. M., Volz, R. K., Bus, V. G. M., & Chagné, D. (2012). Towards genomic selection in apple (Malus × domestica Borkh) breeding programmes: Prospects challenges and strategies. Tree Genetics and Genomes, 8, 1–14. https://doi.org/10.1007/s11295-011-0425-z
Li, J., & Chase, H. A. (2010). Applications of membrane techniques for purification of natural products. Biotechnology Letters, 32, 601–608. https://doi.org/10.1007/s10529-009-0199-7
Lima, L. G. B., Montenegro, J., Pimentel de Abreu, J., Barros Santos, M. C., Pimenta do Nascimento, T., Santos, M., Ferreira, A. G., Cameron, L. C., Ferreira, M. S. L., & Teodoro, A. J. (2020). Metabolite profiling by UPLC-MSE, NMR, and antioxidant properties of Amazonian fruits: Mamey apple (Mammea americana) Camapu (Physalis angulata) and Uxi (Endopleura uchi). Molecules, 25(2), 342. https://doi.org/10.3390/molecules25020342
Mamat, S. F., Azizan, K. A., Baharum, S. N., Noor, N. M., & Aizat, W. M. (2020). GC-MS and LC-MS analyses reveal the distribution of primary and secondary metabolites in mangosteen (Garcinia mangostana Linn) fruit during ripening. Scientia Horticulturae, 262, 109004. https://doi.org/10.1016/j.scienta.2019.109004
Marshall, D. D., & Powers, R. (2017). Beyond the paradigm: Combining mass spectrometry and nuclear magnetic resonance for metabolomics. Progress in Nuclear Magnetic Resonance Spectroscopy, 100, 1–16. https://doi.org/10.1016/j.pnmrs.2017.01.001
Mohammad, A. W., Teow, Y. H., Ang, W. L., Chung, Y. T., Oatley-Radcliffe, D. L., & Hilal, N. (2015). Nanofiltration membranes review: Recent advances and future prospects. Desalination, 356, 226–254. https://doi.org/10.1016/j.desal.2014.10.043
Nath, K., Dave, H. K., & Patel, T. M. (2018). Revisiting the recent applications of nanofiltration in food processing industries: Progress and prognosis. Trends in Food Science & Technology, 73, 12–24. https://doi.org/10.1016/B978-0-12-815866-1.00003-0
Nghiem, L. D., & Hawkes, S. (2007). Effects of membrane fouling on the nanofiltration of pharmaceutically active compounds (PhACs): Mechanisms and role of membrane pore size. Separation and Purification Technology, 57(1), 176–184. https://doi.org/10.1016/j.seppur.2007.04.002
Olennikov, D. N., Vasilieva, A. G., & Chirikova, N. K. (2020). Fragaria viridis fruit metabolites: Variation of LC-MS profile and antioxidant potential during ripening and storage. Pharmaceuticals, 13(9), 262. https://doi.org/10.3390/ph13090262
Paul, M., & Jons, S. D. (2016). Chemistry and fabrication of polymeric nanofiltration membranes: A review. Polymer, 103, 417–456. https://doi.org/10.1016/j.polymer.2016.07.085
Pereira, G. E., Gaudillere, J.-P., Van Leeuwen, C., Hilbert, G., Maucourt, M., Deborde, C., Moing, A., & Rolin, D. (2005). 1H NMR metabolite fingerprints of grape berry: Comparison of vintage and soil effects in Bordeaux grapevine growing areas. Analytica Chimica Acta, 563(1–2), 346–352. https://doi.org/10.1016/j.aca.2005.11.007
Pirlak, L., Ünüvar, G., & Ersoy, N. (2017). Determination of antioxidant activities of some apple cultivars. Horticultural Science, 44(3), 120–125. https://doi.org/10.17221/276/2015-HORTSCI
R Core Team. (2019). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
Rana, S., & Bhushan, S. (2016). Apple phenolics as nutraceuticals: Assessment, analysis and application. Journal of Food Science and Technology, 53(4), 1727–1738. https://doi.org/10.1007/s13197-015-2093-8
TopSpin. (2018). https://www.bruker.com/en/products-and-solutions/mr/nmr-software/topspin.html
Salehi, F. (2014). Current and future applications for nanofiltration technology in the food processing. Food and Bioproducts Processing, 92(C2), 161–177. https://doi.org/10.1016/j.fbp.2013.09.005
Salvino, R., Colella, M., & De Luca, G. (2021). NMR-based metabolomics analysis of Calabrian citrus fruit juices and its application to industrial process quality control. Food Control, 121, 107619. https://doi.org/10.1016/j.foodcont.2020.107619
Santucci, C., Brizzolara, S., & Tenori, L. (2015). Comparison of frozen and fresh apple pulp for NMR-based metabolomic analysis. Food Analytical Method, 8, 2135–2140. https://doi.org/10.1007/s12161-015-0107-9
Seger, C., & Sturm, S. (2007). Analytical aspects of plant metabolite profiling platforms: Current standings and future aim. Journal of Proteome Research, 6(2), 480–497. https://doi.org/10.1021/pr0604716
Sobolev, A. P., Mannina, L., Proietti, N., Carradori, S., Daglia, M., Giusti, A. M., Antiochia, R., & Capitani, D. (2015). Untargeted NMR-based methodology in the study of fruit metabolites. Molecules, 20(3), 4088–4108. https://doi.org/10.3390/molecules20034088
Tallapally, M., Sadiq, A. S., Mehtab, V., Chilakala, S., Vemula, M., Chenna, S., & Upadhyayula, V. (2020). GC-MS based targeted metabolomics approach for studying the variations of phenolic metabolites in artificially ripened banana fruits. LWT - Food Science and Technology, 130, 109622. https://doi.org/10.1016/j.lwt.2020.109622
Ting, V. J. L., Silcock, P., Bremer, P. J., & Biasioli, F. (2013). X-ray micro-computer tomographic method to visualize the microstructure of different apple cultivars. Journal of Food Science, 78(11), E1735–E1742. https://doi.org/10.1111/1750-3841.12290
Tomita, S., Nemoto, T., Matsuo, Y., Shoji, T., Tanaka, F., Nakagawa, H., Ono, H., Kikuchi, J., Ohnishi-Kameyama, M., & Sekiyama, Y. (2015). A NMR-based, non-targeted multistep metabolic profiling revealed L-rhamnitol as a metabolite that characterised apples from different geographic origins. Food Chemistry, 174, 163–172. https://doi.org/10.1016/j.foodchem.2014.11.028
Tundis, R., Conidi, C., Loizzo, M. R., Sicari, V., & Cassano, A. (2020). Olive mill wastewater polyphenol-enriched fractions by integrated membrane process: A promising source of antioxidant, hypolipidemic and hypoglycaemic compounds. Antioxidants, 9(7), 602. https://doi.org/10.3390/antiox9070602
Uyttebroek, M., Vandezande, P., Van Dael, M., Vloemans, S., Noten, B., Bongers, B., Porto-Carrero, W., Unamunzaga, M. M., Bulut, M., & Lemmens, B. (2017). Concentration of phenolic compounds from apple pomace extracts by nanofiltration at lab and pilot scale with a techno-economic assessment. Journal of Food Process Engineering, 41(1), e12629. https://doi.org/10.1111/jfpe.12629
Vermathen, M., Marzorati, M., Baumgartner, D., Good, C., & Vermathen, P. (2011). Investigation of different apple cultivars by high resolution magic angle spinning NMR. A feasibility study. Journal of Agricultural and Food Chemistry, 59(24), 12784–12793. https://doi.org/10.1021/jf203733u
Vermathen, M., Marzoratia, M., & Vermathen, P. (2012). Exploring high-resolution magic angle spinning (HR-MAS) NMR spectroscopy for metabonomic analysis of apples. CHIMIA International Journal for Chemistry, 66(10), 747–751. https://doi.org/10.2533/chimia.2012.747
Acknowledgements
The authors thank Gioia Succhi srl for collecting and supplying samples of Royal Gala, Pink Lady, Golden Delicious, and Fuji apple juices.
Funding
This work was supported by the University of Calabria and POR Calabria — FSE/FESR 2014–2020. The authors wish to thank Calabria Regional institution for its financial support through the AgrInfra Calabria POR FESR-FSE Calabria 2014/2020, Action 1.5.1 grant. L.B. thanks Italian Ministry of Education, University and Research for its grant n. AIM1899391–1 in the framework of the project “Azione I.2, Mobilità dei Ricercatori, PON R&I 2014–2020.”
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Martina Gaglianò: investigation, methodology, formal analysis, data curation, writing — original draft. Carmela Conidi: investigation, methodology, formal analysis. Lucia Bartella: investigation, methodology, formal analysis; Rosachiara A. Salvino: investigation, methodology, formal analysis; Leonardo Di Donna: supervision, conceptualization, data curation, investigation, methodology, writing — original draft; Alfredo Cassano: supervision, conceptualization, data curation, investigation, methodology, writing — original draft, writing — review and editing; Giuseppina De Luca: supervision, conceptualization, data curation, investigation, methodology, writing — original draft, writing — review and editing.
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Gaglianò, M., Conidi, C., Bartella, L. et al. An Integrated Approach Based on NMR and HPLC–UV-ESI–MS/MS to Characterize Apple Juices and Their Nanofiltration (NF) Bioactive Extracts. Food Bioprocess Technol 14, 2273–2285 (2021). https://doi.org/10.1007/s11947-021-02718-8
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DOI: https://doi.org/10.1007/s11947-021-02718-8