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Cite This: J. Agric. Food Chem. 2018, 66, 661−673

Comprehensive Characterization of Extractable and Nonextractable Phenolic Compounds by High-Performance Liquid Chromatography−Electrospray Ionization−Quadrupole Time-ofFlight of a Grape/Pomegranate Pomace Dietary Supplement Iza F. Pérez-Ramírez,†,‡ Rosalía Reynoso-Camacho,† Fulgencio Saura-Calixto,‡ and Jara Pérez-Jiménez*,‡

J. Agric. Food Chem. 2018.66:661-673. Downloaded from pubs.acs.org by UNIV OF GOTHENBURG on 01/23/19. For personal use only.

†

Research and Graduate Studies in Food Science, Facultad de Química, Universidad Autónoma de Querétaro, Cerro de las Campanas s/n, 76010 Santiago de Querétaro, Querétaro, México ‡ Department of Metabolism and Nutrition, Institute of Food Science, Technology and Nutrition (ICTAN-CSIC), José Antonio Novais 10, 28040 Madrid, Spain S Supporting Information *

ABSTRACT: Grape and pomegranate are rich sources of phenolic compounds, and their derived products could be used as ingredients for the development of functional foods and dietary supplements. However, the profile of nonextractable or macromolecular phenolic compounds in these samples has not been evaluated. Here, we show a comprehensive characterization of extractable and nonextractable phenolic compounds of a grape/pomegranate pomace dietary supplement using highperformance liquid chromatography−electrospray ionization−quadrupole time-of-flight (HPLC−ESI−QTOF) and matrixassisted laser desorption/ionization (MALDI)-TOF techniques. The main extractable phenolic compounds were several anthocyanins (principally malvidin 3-O-glucoside) as well as gallotannins and gallagyl derivatives; some phenolic compounds were reported in grape or pomegranate for the first time. Additionally, there was a high proportion of nonextractable phenolic compounds, including vanillic acid, and dihydroxybenzoic acid. Unidentified polymeric structures were detected by MALDI-TOF MS analysis. This study shows that mixed grape and pomegranate pomaces are a source of different classes of phenolic compounds including a high proportion of nonextractable phenolic compounds. KEYWORDS: grape, pomegranate, pomaces, phenolic compounds, ellagitannins, mass spectrometry

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INTRODUCTION Grapes (Vitis vinifera L.) are the largest fruit crop in the world, with annual production of around 75 million tons, mainly used to make wine.1 Meanwhile, pomegranate (Punica granatum L.) annual production is some 1.5 million tons and is consumed fresh or used in the elaboration of juices and jams. Interestingly, pomegranate production has grown steadily in recent years,2 probably due to consumer awareness of the health benefits associated with its consumption. Indeed, both these fruits contain high levels of phenolic compounds, known for their health-related properties, and in fact the two present complementary profiles: red grape is rich in polymeric flavanols or proanthocyanidins, while the most characteristic phenolic compounds in pomegranate are ellagitannins. Furthermore, both contain other flavonoids, such as anthocyanins or flavonols, as well as phenolic acids.3,4 The complementary profile of phenolic compounds in both fruits makes it especially interesting to prepare products combining both of them since they would provide a whole diversity of phenolic compounds. Indeed, phenolic compounds have been suggested to exhibit class-specific effects such as those attributed to the microbialderived metabolites of ellagitannins present in pomegranate5 or to those derived from proanthocyanidins found in grape.6 A huge amount of grape and pomegranate pomace is generated during the industrial processing of these fruits, which is mainly composed of remnant pulp, seeds, and peel. Mass © 2017 American Chemical Society

spectrometry (MS) coupled to liquid chromatography (LC) has been used to identify phenolic acids and flavonoids in grape pomace.3,7 Regarding pomegranate pomace, only some specific phenolic compounds have been measured by high-performance liquid chromatography (HPLC)−diode-array detection (DAD),8 while detailed HPLC−MS analysis, including that of low-molecular-weight (8 ppm); however, MS/MS fragments are characteristics of the suggested compound. cMS/MS fragments obtained from the analysis of EP fraction. a

Figure 2. Identification of petunidin 3-O-(6″-coumaroyl-glucoside) (m/z 625.1558, No. 13) by HPLC−ESI−QTOF in positive mode in the extractable phenolic compounds fraction of a grape/pomegranate pomaces dietary supplement: (A) MS spectrum; (B) MS/MS spectrum (18.9 min).

and pedunculagin. Although only two punicalagin isomers have commonly been reported,46 we identified three apparent punicalagin signals, which concur with a recent study reporting four isomers of punicalagin.9 Also, several isomers were found for punicalin and peduncalagin, as previously reported.4,47 Two signals were detected for gallogyl-HHDP-hexoside (m/z 633), which may correspond to corilagin, strictin, or punicacortein, depending on the linkages.48 Greater extraction of several ellagitannins was achieved from the extractable ellagitannins fraction than the extractable phenolic compounds fraction, as expected, the former showing

a higher content of punicalin and punicalagins (27%−42%). Moreover, granatin B (m/z 951, showing a fragment at 301 that corresponds to ellagic acid) another major ellagitannin in pomegranate11,40 was also detected at higher concentrations in the extractable ellagitannins fraction. Two additional ellagitannins were found in this fraction: brevifolin carboxylic acid, previously reported in pomegranate,4 and an unknown compound with m/z 663, which was included in this group due to fragments that are characteristic of this class. Additionally, three flavonoids were only detected in the extractable ellagitannins fraction: malvidin-3-O-(6″-coumaroyl668

DOI: 10.1021/acs.jafc.7b05901 J. Agric. Food Chem. 2018, 66, 661−673

Article

Journal of Agricultural and Food Chemistry

Figure 3. Identification of two isomers of dicaffeoylquinic acid (m/z 517, No. 33) by HPLC−ESI−QTOF in positive mode in the extractable phenolic compounds fraction of a grape/pomegranate pomaces dietary supplement: (A) MS spectrum; (B) MS/MS spectrum at 13.30 min; (C) MS/MS spectrum at 13.55 min. Both isomers are depicted with the same structure since it was not possible to ascertain the specific structure of each isomer.

reported in grape products, a previous study with another grape pomace did not find stilbenes;49 similarly to this one, grape pomace was collected after complete wine fermentation, which may explain this result. Nonextractable Fraction. Sixty-one different compounds were found in the nonextractable fraction (hydrolyzable phenolic compounds and nonextractable ellagitannins) of the grape/pomegranate dietary supplement, from which only 11 compounds were identified as phenolic compounds by analyzing their exact mass and fragmentation pattern. Table 4 shows the compounds which were identified. Seven phenolic compounds were only identified in the hydrolyzable phenolic compounds fraction, mainly phenolic acids; two hydroxyben-

glucoside) quercetin 3-O-glucoside (also known as isoquercetin), and kaempferol, all of which are characteristic of red grape pomace.3 Stilbenes were searched in the extractable fraction (both extractable and hydrolyzable phenolic compounds fractions). In particular, the following m/z were extracted from the total ion chromatogram in the negative mode: 453 (δ-viniferin, εviniferin, and pallidol), 243 (piceatannol), 405 (piceatannol 3O-glucoside), 227 (resveratrol), and 289 (resveratrol 3-Oglucoside). None of them was detected. In contrast, resveratrol standard was detected at 0.5 ppm in the same conditions. Therefore, the sample did not contain stilbenes or only as traces. Although this class of phenolic compounds has been 669


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Table 4. HPLC−ESI−QTOF Profile of Hydrolyzable Phenolic Compounds and Nonextractable Ellagitannin Fractions of a Grape/Pomegranate Pomaces Dietary Supplementa no.

retention time (min)

proposed compound

Hydrolyzable Phenolic Compounds Fraction Flavanones 59 24.17 pinocembrin Hydroxybenzoic Acids 60 12.48 methyl gallate 61 17.39 vanillic acid Hydroxycinnamic Acids 62 23.13 ferulic acid Hydroxyciynnamaldehydes 63 27.38 ferulaldehyde Hydroxyphenylpropanoic Acids 64 15.34 3-(3,4-dihydroxyphenyl)-2methoxy propionic acid Ellagitannins 37 19.88 ellagic acid 44 11.93 galloyl-HHDP-glucoside (lagerstannin C) Nonextractable Ellagitannins Fraction Hydroxybenzoic Acids 65 11.77 hydroxybenzoic acid 66 9.73 dihydroxybenzoic acid 61 17.28 vanillic acid a

ionization

experimental mass

calculated mass

ppm

formula

amount (mg/ 100 g dw)

ESI−

255.0668

111, 113, 161

255.0663

−2.02

C15H12O4

0.4 ± 0.04

ESI− ESI−

183.0295 167.0348

101, 111, 124, 165 111, 113, 126, 161

183.0299 167.0350

2.16 1.08

ESI−

193.0512

101, 111, 113, 133, 161, 179

193.0506

ESI−

177.0557

111, 161

ESI−

211.0623

ESI− ESI−

ESI− ESI− ESI−

MS/MS ions

C8H8O5 C8H8O4

52.1 ± 5.6 40.7 ± 6.7

−2.93

C10H10O4

20.1 ± 4.7

177.0557

0.10

C10H10O3

61.8 ± 8.9

111, 113, 126

211.0612

5.20

C10H12O5

3.6 ± 1.0

300.999 649.0685

101,185, 229 113, 361, 481, 557

300.9990 549.0683

−3.01 −0.83

C14H6O8 C27H22O19

7.9 ± 0.2 5.2 ± 1.7

137.0243 153.0197 167.0353

113 109, 113, 125 113, 135

137.0244 153.0193 167.0350

0.85 −2.39 −1.89

C7H6O3 C7H6O4 C8H8O4

4.8 ± 0.7 74.3 ± 9.0 2.2 ± 0.3

Data are expressed as mean ± standard error (n = 3). HHDP, hexahydroxydiphenic acid.

corresponds to a fragment of caffeic acid hexoside, reported in the nonextractable fraction of pomegranate;9 when this signal is detected as MS/MS ions, it could correspond to a derivative. Therefore, there is a need to advance methodologies that allow nonextractable phenolic compounds to be released from the food matrix while reducing degradation of their original phenolic structures; this is especially relevant considering the increasing evidence of the health-related properties of these compounds.31 Moreover, methods to analyze intact nonextractable proanthocyanidins are needed since once the butanolysis treatment is performed, only derived anthocyanins can be detected. MALDI-TOF MS Profile. High-molecular-weight polymeric phenolic compounds are poorly separated in reversed-phase LC; therefore, the extractable phenolic compounds and extractable ellagitannins fractions were also analyzed by MALDI-TOF MS, a technique that has been successfully used for the identification of proanthocyanidins constituted of up to several dozen units12 and rarely used for the characterization of ellagitannins15 or anthocyanins.14 When it was applied to the extractable phenolic compounds and extractable ellagitannins fractions of the dietary supplement, the spectra showed a classic polymeric distribution in an m/z range from 388 to 2476 ([M+ Na]+) for the extractable phenolic compounds fraction and from 1571 to 2695 ([M+ H]+) for the extractable ellagitannins fraction. In both fractions, the separation between signals was of 224 units (in the extractable ellagitannins fraction it was 226 in some cases), with nine signals corresponding to different degrees of polymerization in the extractable phenolic compounds fraction and eight in the extractable ellagitannins fraction, although the starting mass was different in each fraction. These separations could correspond to a phenolic acid with a molecular weight of 242 Da, losing a water molecule on release from the polymeric

zoic acids were identified only in the nonextractable ellagitannins fraction; and one hydroxybenzoic acid (vanillic acid) was identified in both fractions (Table 3). Among the molecules identified, only ellagic acid and lagerstannin C were also detected in the extractable fraction. The MS/MS signals for ellagic acid, along with the fragments obtained for the standard, are shown in Figure 4; although this compound is difficult to fragment, characteristics signals corresponding to losses of one CO2 and one CO molecule (m/z 229) as well as of two CO2 and one CO molecule (m/z 185) were observed.4,40 The different profiles of the extractable and nonextractable fractions seem to suggest that some phenolic compounds are only detected after release from macromolecules in the food matrix; this could be the case of ferulic acid, which is known to be associated with the cell wall. Nevertheless, it is important to mention that the drastic acid hydrolysis needed for the release of these molecules from the food matrix may also degrade some of the original phenolic structures.10 Along these lines, the identification of ferulaldehyde in the hydrolyzable phenolic compounds but not in the extractable phenolic compounds fraction of common fruits has been reported, and it has been suggested that this compound might be derived from the degradation of other phenolic compounds, as reported for curcumin.10 This kind of transformation makes the identification of molecular ions detected after hydrolysis difficult since they may correspond to compounds not included in the databases on phenolic compounds. This would explain the low identification rate in these fractions, particularly in the hydrolyzable phenolic compounds fraction. Indeed, some fragments that were repeated in many of the unidentified signals have been reported to be characteristic of pomegranate phenolic compounds, such as m/z 177 from brevifolin carboxylic acid or m/z 243 from punicalin.4 Another repeated fragment, with m/z 161, 670


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Figure 4. Identification of ellagic acid (No. 37) by HPLC−ESI−QTOF in negative mode in the hydrolyzable phenolic compounds fraction of a grape/pomegranate pomaces dietary supplement: (A) MS spectrum at m/z 301, corresponding to ellagic acid eluted in a standards mixture; (B) MS spectrum at m/z 301 for the sample; (C) MS/MS spectrum for the fragmentation of m/z 301 (19.98 min) in the standards mixture; (D) MS/MS spectrum for the fragmentation of m/z 301 (19.98 min) in the sample.

structure, or to a flavonoid with a molecular weight of 226 Da, linked by a C−C bound to the polymeric structure. However, from these separations, it was not possible to ascertain the identity of these polymeric structures since they did not seem to correspond to proanthocyanidins, ellagitannins, or anthocyanins. It should be remarked that, although the mean degree of polymerization of proanthocyanidins in grape is up to several dozen units in peel,36 when MALDI-TOF MS was applied to this fruit or its derived products, only hexamers were detected.13 Therefore, some specific optimization may be needed for these samples. Also, we were able to obtain signals using dithranol as a matrix, where other authors have reported it is an invalid matrix for proanthocyanidin analysis;50 therefore, our signals could correspond to other polymeric phenolic compounds. In any case, we consider that the information provided here may be useful in future research to identify polymeric structures in grape or pomegranate products.

In summary, a detailed characterization of phenolic compounds in a grape/pomegranate pomace dietary supplement was carried out by HPLC−ESI−QTOF, including the identification of some phenolic compounds not previously reported in either grape or pomegranate. Our results show this dietary supplement to be a rich source of phenolic compounds belonging to different classes as well as confirming the important contribution of nonextractable phenolic compounds to its total content of phenolic compounds. MALDI-TOF MS analysis showed the presence of unidentified polymeric structures in this dietary supplement. These results highlight the importance of performing comprehensive characterizations of phenolic compounds profiles in natural products including the commonly ignored nonextractable phenolic compounds. 671


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ellagitannins yields two urolithin-metabotypes that correlate with cardiometabolic risk biomarkers: Comparison between normoweight, overweight-obesity and metabolic syndrome. Clin. Nutr. 2017, DOI: 10.1016/j.clnu.2017.03.012. (6) Fernández-Millán, E.; Ramos, S.; Alvarez, C.; Bravo, L.; Goya, L.; Martín, M. T. Microbial phenolic metabolites improve glucosestimulated insulin secretion and protect pancreatic beta cells against tert-butyl hydroperoxide-induced toxicity via ERKs and PKC pathways. Food Chem. Toxicol. 2014, 66, 245−253. (7) Amico, V.; Napoli, E. M.; Renda, A.; Ruberto, G.; Spatafora, C.; Tringali, C. Constituents of grape pomace from the Sicilian cultivar ’Nerello Mascalese’. Food Chem. 2004, 88, 599−607. (8) Surek, E.; Nilufer-Erdil, D. Phenolic contents, antioxidant activities and potential bioaccessibilities of industrial pomegranate nectar processing wastes. Int. J. Food Sci. Technol. 2016, 51, 231−239. (9) Ambigaipalan, P.; De Camargo, A. C.; Shahidi, F. Phenolic compounds of pomegranate byproducts (outer skin, mesocarp, divider membrane) and their antioxidant activities. J. Agric. Food Chem. 2016, 64, 6584−6604. (10) Pérez-Jiménez, J.; Saura Calixto, F. Macromolecular antioxidants or non-extractable polyphenols in fruit and vegetables: intake in four European countries. Food Res. Int. 2015, 74, 315−23. (11) García-Villalba, R.; Espín, J. C.; Aaby, K.; Alasalvar, C.; Heinonen, M.; Jacobs, G.; Voorspoels, S.; Koivumäki, T.; Kroon, P. A.; Pelvan, E.; Saha, S.; Tomás-Barberán, F. A. Validated method for the characterization and quantification of extractable and nonextractable ellagitannins after acid hydrolysis in pomegranate fruits, juices, and extracts. J. Agric. Food Chem. 2015, 63, 6555−6566. (12) Monagas, M.; Quintanilla-López, J. E.; Gómez-Cordovés, C.; Bartolomé, B.; Lebrón-Aguilar, R. MALDI-TOF MS analysis of plant proanthocyanidins. J. Pharm. Biomed. Anal. 2010, 51, 358−372. (13) Vergara-Salinas, J. R.; Bulnes, P.; Zúñiga, M. C.; Pérez-Jiménez, J.; Torres, J. L.; Mateos-Martín, M. L.; Agosin, E.; Pérez-Correa, J. R. Effect of pressurized hot water extraction on antioxidants from grape pomace before and after enological fermentation. J. Agric. Food Chem. 2013, 61, 6929−6936. (14) Oliveira, J.; Alhinho Da Silva, M.; Teixeira, N.; De Freitas, V.; Salas, E. Screening of anthocyanins and anthocyanin-derived pigments in red wine grape pomace using LC-DAD/MS and MALDI-TOF techniques. J. Agric. Food Chem. 2015, 63, 7636−7644. (15) Hager, T. J.; Howard, L. R.; Liyanage, R.; Lay, J. O.; Prior, R. L. Ellagitannin composition of blackberry as determined by HPLC-ESIMS and MALDI-TOF-MS. J. Agric. Food Chem. 2008, 56, 661−669. (16) Medjakovic, S.; Jungbauer, A. Pomegranate: A fruit that ameliorates metabolic syndrome. Food Funct. 2013, 4, 19−39. (17) Akaberi, M.; Hosseinzadeh, H. Grapes (Vitis vinifera) as a potential candidate for the therapy of the metabolic syndrome. Phytother. Res. 2016, 30, 540−556. (18) National Library of Medicine Clinical Trials.gov; U.S. National Library of Medicine, 2017. www.clinicaltrials.gov (accessed December 21, 2017). (19) Pérez-Jiménez, J.; Arranz, S.; Tabernero, M.; Díaz- Rubio, M. E.; Serrano, J.; Goñi, I.; Saura-Calixto, F. Updated methodology to determine antioxidant capacity in plant foods, oils and beverages: Extraction, measurement and expression of results. Food Res. Int. 2008, 41, 274−285. (20) Arranz, S.; Saura-Calixto, F.; Shaha, S.; Kroon, P. A. High contents of nonextractable polyphenols in fruits suggest that polyphenol contents of plant foods have been underestimated. J. Agric. Food Chem. 2009, 57, 7298−7303. (21) Hartzfeld, P. W.; Forkner, R.; Hunter, M. D.; Hagerman, A. E. Determination of hydrolyzable tannins (gallotannins and ellagitannins) after reaction with potassium iodate. J. Agric. Food Chem. 2002, 50, 1785−1790. (22) Pérez-Jiménez, J.; Arranz, S.; Saura-Calixto, F. Proanthocyanidin content in foods is largely underestimated in the literature data: An approach to quantification of the missing proanthocyanidins. Food Res. Int. 2009, 42, 1381−1388.

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.7b05901. MS/MS data (ESI−) of nonidentified compounds of HP and NEET fractions of grape/pomegranate pomaces dietary supplement; MALDI-TOF MS analysis of extractable polyphenols fraction of a grape/pomegranate pomaces dietary supplement; MALDI-TOF MS analysis of extractable ellagitannins fraction of a grape/pomegranate pomaces dietary supplement (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: (+34) 91 549 23 00. Fax: (+34) 91 549 36 27. ORCID

Jara Pérez-Jiménez: 0000-0002-2811-4558 Funding

Spanish Ministry of Science and Innovation (Grant No. AGL2014−55102-JIN). The authors are grateful for the CONACyT for the international scholarship granted to I.F.P.R. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We are grateful to the ICTAN Analysis Services Unit for providing facilities for chromatography analysis and in particular to Dr. Inmaculada Á lvarez-Acero for technical assistance. We thank the Mass Spectrometry Center (Complutense University of Madrid) for providing facilities and technical assistance for MALDI-TOF MS analysis, in particular to Dr. Cristina Gutiérrez-López and Estefanı ́a Garcı ́aCalvo. Vitalgrana S. A. and Roquesan Wineries are grateful for kindly providing the raw materials.

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ABBREVIATIONS USED ABTS, 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid); DHHDP, dehydro-hexahydroxydiphenic acid; FRAP, ferric reducing/antioxidant power; HHDP, hexahydroxydiphenic acid; MALDI, matrix-assisted laser desorption ionization; QTOF, quadrupole−time-of-flight; RDA, retro-Diels−Alder; TOF, time-of-flight

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REFERENCES

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