Phenolic Compounds of Pomegranate Byproducts (Outer Skin, Mesocarp, Divider Membrane) and Their Antioxidant Activities

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 34, 2016, Pages 6584-6604

  Ambigaipalan, Priyatharini ^a   De Camargo, Adriano Costa ^a,b   Shahidi, Fereidoon ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

antioxidant activity; divider membrane; insoluble bound; mesocarp; outer skin; phenolic compounds; pomegranate

Indexed keywords

ANTIOXIDANTS; BYPRODUCTS; FLAVONOIDS; FREE RADICALS; PHENOLS; TANNINS;

ANTI-OXIDANT ACTIVITIES; INSOLUBLE-BOUND; MESOCARP; PHENOLIC COMPOUNDS; POMEGRANATE;

PLANTS (BOTANY);

ANTIOXIDANT; PHENOL DERIVATIVE; PLANT EXTRACT; WASTE;

ANALYSIS; CHEMISTRY; FRUIT; LYTHRACEAE; WASTE;

ANTIOXIDANTS; FRUIT; PHENOLS; PLANT EXTRACTS; PUNICACEAE; WASTE PRODUCTS;

EID: 84984829640     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b02950     Document Type: Article

References (80)

1. Glozer, K.; Ferguson, L. Pomegranate Production in Afghanistan; Bell, M., Ed.; Department of Plant Sciences, College of Agricultural and Environmental Sciences, University of California: Davis, CA, USA; http://afghanag.ucdavis.edu/a-horticulture/fruits-trees/pomegranate/Pomegranate%20manuals/Pomegranate-manual.pdf, cited Nov 17, 2015.
2. n. Food Chem. 2016, submitted for publication
3. Putta, S.; Kilari, E. K. Protective activity of aqueous pericarp extract of Punica granatum against hyperglycaemia induced by streptozotocin in rats Biosci., Biotechnol. Res. Asia 2014, 11, 1439-1446 10.13005/bbra/1536
4. Duke, J. A.; Ayensu, E. S. Medicinal Plants of China; Reference Publications: Algonac, MI, USA, 1985; p 705.
5. Aviram, M.; Volkova, N.; Coleman, R.; Dreher, M.; Reddy, M. K.; Ferreira, D.; Rosenblat, M. Pomegranate phenolics from the peels, arils, and flowers are antiatherogenic: studies in vivo in atherosclerotic apolipoprotein E-deficient (E0) mice and in vitro in cultured macrophages and lipoproteins J. Agric. Food Chem. 2008, 56, 1148-1157 10.1021/jf071811q
6. Toi, M.; Bando, H.; Ramachandran, C.; Melnick, S. J.; Imai, A.; Fife, R. S.; Carr, R. E.; Oikawa, T.; Lansky, E. P. Preliminary studies on the anti-angiogenic potential of pomegranate fractions in vitro and in vivo Angiogenesis 2003, 6, 121-128 10.1023/B:AGEN.0000011802.81320.e4
7. Liu, W.; Ma, H.; Frost, L.; Yuan, T.; Dain, J. A.; Seeram, N. P. Pomegranate phenolics inhibit formation of advanced glycation end products by scavenging reactive carbonyl species Food Funct. 2014, 5, 2996-3004 10.1039/C4FO00538D
8. Faria, A.; Monteiro, R.; Mateus, N.; Azevedo, I.; Calhau, C. Effect of pomegranate (Punica granatum) juice intake on hepatic oxidative stress Eur. J. Nutr. 2007, 46, 271-278 10.1007/s00394-007-0661-z
9. Dikmen, M.; Ozturk, N.; Ozturk, Y. The antioxidant potency of Punica granatum L. fruit peel reduces cell proliferation and induces apoptosis on breast cancer J. Med. Food 2011, 14, 1638-1646 10.1089/jmf.2011.0062
10. Wu, D.; Ma, X.; Tian, W. Pomegranate husk extract, punicalagin and ellagic acid inhibit fatty acid synthase and adipogenesis of 3T3-L1 adipocyte J. Funct. Foods 2013, 5, 633-641 10.1016/j.jff.2013.01.005
11. Adams, L. S.; Seeram, N. P.; Aggarwal, B. B.; Takada, Y.; Sand, D.; Heber, D. Pomegranate juice, total pomegranate ellagitannins, and punicalagin suppress inflammatory cell signaling in colon cancer cells J. Agric. Food Chem. 2006, 54, 980-985 10.1021/jf052005r
12. Hong, M. Y.; Seeram, N. P.; Heber, D. Pomegranate polyphenols down-regulate expression of androgen-synthesizing genes in human prostate cancer cells overexpressing the androgen receptor J. Nutr. Biochem. 2008, 19, 848-855 10.1016/j.jnutbio.2007.11.006
13. 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. 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 10.1021/acs.jafc.5b02062
14. Noda, Y.; Kaneyuki, T.; Mori, A.; Packer, L. Antioxidant activities of pomegranate fruit extract and its anthocyanidins: delphinidin, cyanidin, and pelargonidin J. Agric. Food Chem. 2002, 50, 166-171 10.1021/jf0108765
15. Singh, R. P.; Chidambara Murthy, K. N.; Jayaprakasha, G. K. Studies on the antioxidant activity of pomegranate (Punica granatum) peel and seed extracts using in vitro models J. Agric. Food Chem. 2002, 50, 81-86 10.1021/jf010865b
16. Negi, P. S.; Jayaprakasha, G. K.; Jena, B. S. Antioxidant and antimutagenic activities of pomegranate peel extracts Food Chem. 2003, 80, 393-397 10.1016/S0308-8146(02)00279-0
17. Li, Y.; Guo, C.; Yang, J.; Wei, J.; Xu, J.; Cheng, S. Evaluation of antioxidant properties of pomegranate peel extract in comparison with pomegranate pulp extract Food Chem. 2006, 96, 254-260 10.1016/j.foodchem.2005.02.033
18. Qu, W.; Pan, Z.; Ma, H. Extraction modeling and activities of antioxidants from pomegranate marc J. Food Eng. 2010, 99, 16-23 10.1016/j.jfoodeng.2010.01.020
19. Wang, Z.; Pan, Z.; Ma, H.; Atungulu, G. G. Extract of phenolics from pomegranate peels Open Food Sci. J. 2011, 5, 17-25 10.2174/1874256401105010017
20. Abbas, M. N. Pomegranate peels: source of antioxidants extraction and natural dentifrices preparation Eur. Academic Res. 2014, 2, 3078-3089
21. Shahidi, F.; Ambigaipalan, P. Phenolics and polyphenolics in foods, beverages and spices: antioxidant activity and health effects-A review J. Funct. Foods 2015, 18, 820-897 10.1016/j.jff.2015.06.018
22. CÌam, M.; ErdogIan, F.; Aslan, D.; Dinç, M. Enrichment of functional properties of ice cream with pomegranate by-products J. Food Sci. 2013, 78, C1543-C1550 10.1111/1750-3841.12258
23. Mosele, J. I.; Macià, A.; Romero, M. P.; Motilva, M. J.; Rubió, L. Application of in vitro gastrointestinal digestion and colonic fermentation models to pomegranate products (juice, pulp and peel extract) to study the stability and catabolism of phenolic compounds J. Funct. Foods 2015, 14, 529-540 10.1016/j.jff.2015.02.026
24. Qin, Y. Y.; Zhang, Z. H.; Li, L.; Xiong, W.; Shi, J. Y.; Zhao, T. R.; Fan, J. Antioxidant effect of pomegranate rind powder extract, pomegranate juice, and pomegranate seed powder extract as antioxidants in raw ground pork meat Food Sci. Biotechnol. 2013, 22, 1063-1069 10.1007/s10068-013-0184-8
25. Singleton, V. L.; Rossi, J. A. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents Am. J. Enol. Vitic. 1965, 16, 144-158
26. Giusti, M. M.; Wrolstad, R. E. Unit F1.2.1-13. Anthocyanins. Characterization and measurement with UV visible spectroscopy. In Current Protocols in Food Analytical Chemistry; Wrolstad, R. E., Ed.; Wiley, New York, 2011; pp 1-13.
27. Chandrasekara, A.; Shahidi, F. Determination of antioxidant activity in free and hydrolyzed fractions of millet grains and characterization of their phenolic profiles by HPLC-DAD-ESI-MS n J. Funct. Foods 2011, 3, 144-158 10.1016/j.jff.2011.03.007
28. Ambigaipalan, P.; Shahidi, F. Date seed flour and hydrolysates affect physicochemical properties of muffin Food Biosci. 2015, 12, 54-60 10.1016/j.fbio.2015.06.001
29. Ambigaipalan, P.; Al-Khalifa, A. S.; Shahidi, F. Antioxidant and angiotensin I converting enzyme (ACE) inhibitory activities of date seed protein hydrolysates prepared using Alcalase, Flavourzyme and Thermolysin J. Funct. Foods 2015, 18, 1125-1137 10.1016/j.jff.2015.01.021
30. Eom, S. H.; Lee, S. H.; Yoon, N. Y.; Jung, W. K.; Jeon, Y. J.; Kim, S. K.; Lee, M. S.; Kim, Y. M. α-Glucosidase-and α-amylase-inhibitory activities of phlorotannins from Eisenia bicyclis J. Sci. Food Agric. 2012, 92, 2084-2090 10.1002/jsfa.5585
31. Marrelli, M.; Menichini, F.; Statti, G. A.; Bonesi, M.; Duez, P.; Menichini, F.; Conforti, F. Changes in the phenolic and lipophilic composition, in the enzyme inhibition and antiproliferative activity of Ficus carica L. cultivar Dottato fruits during maturation Food Chem. Toxicol. 2012, 50, 726-733 10.1016/j.fct.2011.12.025
32. Ambigaipalan, P.; Shahidi, F. Antioxidant potential of date (Phoenix dactylifera L.) seed protein hydrolysates and carnosine in food and biological systems J. Agric. Food Chem. 2015, 63, 864-871 10.1021/jf505327b
33. de Camargo, A. C.; Regitano-d'Arce, M. A. B.; Biasoto, A. C. T.; Shahidi, F. Low molecular weight phenolics of grape juice and winemaking byproducts: antioxidant activities and inhibition of oxidation of human low-density lipoprotein cholesterol and DNA strand breakage J. Agric. Food Chem. 2014, 62, 12159-12171 10.1021/jf504185s
34. n Food Chem. 2011, 127, 807-821 10.1016/j.foodchem.2010.12.156
35. Aviram, M.; Dornfeld, L.; Kaplan, M.; Coleman, R.; Gaitini, D.; Nitecki, S.; Hofman, A.; Fuhrman, B. Pomegranate juice flavonoids inhibit low-density lipoprotein oxidation and cardiovascular diseases: studies in atherosclerotic mice and in humans Drugs Exp. Clin. Res. 2001, 28, 49-62
36. Viuda-Martos, M.; Ruiz-Navajas, Y.; Fernández-López, J.; Sendra, E.; Sayas-Barberá, E.; Pérez-álvarez, J. A. Antioxidant properties of pomegranate (Punica granatum L.) bagasses obtained as co-product in the juice extraction Food Res. Int. 2011, 44, 1217-1223 10.1016/j.foodres.2010.10.057
37. Elfalleh, W.; Hannachi, H.; Tlili, N.; Yahia, Y.; Nasri, N.; Ferchichi, A. Total phenolic contents and antioxidant activities of pomegranate peel, seed, leaf and flower J. Med. Plants Res. 2012, 6, 4724-4730 10.5897/JMPR11.995
38. Lee, J.; Durst, R. W.; Wrolstad, R. E. Determination of total monomeric anthocyanin pigment content of fruit juices, beverages, natural colorants, and wines by the pH differential method: collaborative study J. AOAC Int. 2005, 88, 1269-1278
39. Yamaguchi, T.; Takamura, H.; Matoba, T.; Terao, J. HPLC method for evaluation of the free radical-scavenging activity of foods by using 1,1-diphenyl-2-picrylhydrazyl Biosci., Biotechnol., Biochem. 1998, 62, 1201-1204 10.1271/bbb.62.1201
40. Tzulker, R.; Glazer, I.; Bar-Ilan, I.; Holland, D.; Aviram, M.; Amir, R. Antioxidant activity, polyphenol content, and related compounds in different fruit juices and homogenates prepared from 29 different pomegranate accessions J. Agric. Food Chem. 2007, 55, 9559-9570 10.1021/jf071413n
41. Amarowicz, R.; Pegg, R. B.; Rahimi-Moghaddam, P.; Barl, B.; Weil, J. A. Free-radical scavenging capacity and antioxidant activity of selected plant species from the Canadian prairies Food Chem. 2005, 84, 551-562 10.1016/S0308-8146(03)00278-4
42. Je, J.-Y.; Park, P.-J.; Kim, S.-K. Antioxidant activity of a peptide isolated from Alaska pollack (Theragra chalcogramma) frame protein hydrolysate Food Res. Int. 2005, 38, 45-50 10.1016/j.foodres.2004.07.005
43. Huang, D.; Ou, B.; Prior, R. L. The chemistry behind antioxidant capacity assays J. Agric. Food Chem. 2005, 53, 1841-1856 10.1021/jf030723c
44. Hider, R. C.; Liu, Z. D.; Khodr, H. H. Metal chelation of polyphenols Methods Enzymol. 2005, 335, 190-203 10.1016/S0076-6879(01)35243-6
45. Kam, A.; Li, K. M.; Razmovski-Naumovski, V.; Nammi, S.; Shi, J.; Chan, K.; Li, G. Q. A comparative study on the inhibitory effects of different parts and chemical constituents of pomegranate on α-amylase and α-glucosidase Phytother. Res. 2013, 27, 1614-1620 10.1002/ptr.4913
46. de Camargo, A. C.; Regitano-d'Arce, M. A. B.; Biasoto, A. C. T.; Shahidi, F. Enzyme-assisted extraction of phenolics from winemaking by-products: antioxidant potential and inhibition of α-glucosidase and lipase activities Food Chem. 2016, 212, 395-402 10.1016/j.foodchem.2016.05.047
47. Zhen-jian, X. I. E. Study on effect of pomegranate pind extracts on enzyme inhibitory [J] J. Anhui Agric. Sci. 2009, 7, 003
48. CÌam, M.; Içyer, N. C.; ErdogÌan, F. Pomegranate peel phenolics: microencapsulation, storage stability and potential ingredient for functional food development LWT-Food Sci. Technol. 2014, 55, 117-123 10.1016/j.lwt.2013.09.011
49. Parmar, H. S.; Kar, A. Antidiabetic potential of Citrus sinensis and Punica granatum peel extracts in alloxan treated male mice BioFactors 2007, 31, 17-24 10.1002/biof.5520310102
50. Birari, R. B.; Bhutani, K. K. Pancreatic lipase inhibitors from natural sources: unexplored potential Drug Discovery Today 2007, 12, 879-889 10.1016/j.drudis.2007.07.024
51. Sugiyama, H.; Akazome, Y.; Shoji, T.; Yamaguchi, A.; Yasue, M.; Kanda, T.; Ohtake, Y. Oligomeric procyanidins in apple polyphenol are main active components for inhibition of pancreatic lipase and triglyceride absorption J. Agric. Food Chem. 2007, 55, 4604-4609 10.1021/jf070569k
52. Gholamhoseinian, A.; Shahouzehi, B.; Sharifi-Far, F. Inhibitory effect of some plant extracts on pancreatic lipase Int. J. Pharmacol. 2010, 6, 18-24 10.3923/ijp.2010.18.24
53. Sergent, T.; Vanderstraeten, J.; Winand, J.; Beguin, P.; Schneider, Y. J. Phenolic compounds and plant extracts as potential natural anti-obesity substances Food Chem. 2012, 135, 68-73 10.1016/j.foodchem.2012.04.074
54. Mathew, A. S.; Capel-Williams, G. M.; Berry, S. E.; Hall, W. L. Acute effects of pomegranate extract on postprandial lipaemia, vascular function and blood pressure Plant Foods Hum. Nutr. 2012, 67, 351-357 10.1007/s11130-012-0318-9
55. Chisolm, G. M.; Steinberg, D. The oxidative modification hypothesis of atherogenesis: an overview Free Radical Biol. Med. 2000, 28, 1815-1826 10.1016/S0891-5849(00)00344-0
56. Hu, C.; Kitts, D. D. Evaluation of antioxidant activity of epigallocatechin gallate in biphasic model systems in vitro Mol. Cell. Biochem. 2001, 218, 147-155 10.1023/A:1007220928446
57. Kaplan, M.; Hayek, T.; Raz, A.; Coleman, R.; Dornfeld, L.; Vaya, J.; Aviram, M. Pomegranate juice supplementation to atherosclerotic mice reduces macrophage lipid peroxidation, cellular cholesterol accumulation and development of atherosclerosis J. Nutr. 2001, 131, 2082-2089
58. Guo, S.; Deng, Q.; Xiao, J.; Xie, B.; Sun, Z. Evaluation of antioxidant activity and preventing DNA damage effect of pomegranate extracts by chemiluminescence method J. Agric. Food Chem. 2007, 55, 3134-3140 10.1021/jf063443g
59. Aqil, F.; Munagala, R.; Vadhanam, M. V.; Kausar, H.; Jeyabalan, J.; Schultz, D. J.; Gupta, R. C. Anti-proliferative activity and protection against oxidative DNA damage by punicalagin isolated from pomegranate husk Food Res. Int. 2012, 49, 345-353 10.1016/j.foodres.2012.07.059
60. Shirode, A. B.; Kovvuru, P.; Chittur, S. V.; Henning, S. M.; Heber, D.; Reliene, R. Antiproliferative effects of pomegranate extract in MCF-7 breast cancer cells are associated with reduced DNA repair gene expression and induction of double strand breaks Mol. Carcinog. 2014, 53, 458-470 10.1002/mc.21995
61. de Camargo, A. C.; Regitano-d'Arce, M. A. B.; Gallo, C. R.; Shahidi, F. Gamma-irradiation induced changes in microbiological status, phenolic profile and antioxidant activity of peanut skin J. Funct. Foods 2015, 12, 129-143 10.1016/j.jff.2014.10.034
62. Sanz, M.; Simón, B. F.; Cadahía, E.; Esteruelas, E.; MunÌoz, A. M.; Hernández, T.; Estrella, I.; Pinto, E. LC-DAD/ESI-MS/MS study of phenolic compounds in ash (Fraxinus excelsior L. and F. americana L.) heartwood. Effect of toasting intensity at cooperage J. Mass Spectrom. 2012, 47, 905-918 10.1002/jms.3040
63. Mena, P.; Calani, L.; Dall'Asta, C.; Galaverna, G.; García-Viguera, C.; Bruni, R.; Crozier, A.; Del Rio, D. Rapid and comprehensive evaluation of (poly) phenolic compounds in pomegranate (Punica granatum L.) juice by UHPLC-MSn Molecules 2012, 17, 14821-14840 10.3390/molecules171214821
64. Zhao, Y.; Li, X.; Zeng, X.; Huang, S.; Hou, S.; Lai, X. Characterization of phenolic constituents in Lithocarpus polystachyus Anal. Methods 2014, 6, 1359-1363 10.1039/c3ay41288a
65. He, L.; Xu, H.; Liu, X.; He, W.; Yuan, F.; Hou, Z.; Gao, Y. Identification of phenolic compounds from pomegranate (Punica granatum L.) seed residues and investigation into their antioxidant capacities by HPLC-ABTS(+) assay Food Res. Int. 2011, 44, 1161-1167 10.1016/j.foodres.2010.05.023
66. Sandhu, A. K.; Gu, L. Antioxidant capacity, phenolic content, and profiling of phenolic compounds in the seeds, skin, and pulp of Vitis rotundifolia (muscadine grapes) as determined by HPLC-DAD-ESI-MS n J. Agric. Food Chem. 2010, 58, 4681-4692 10.1021/jf904211q
67. Khanbabaee, K.; van Ree, T. Tannins: classification and definition Nat. Prod. Rep. 2001, 18, 641-649 10.1039/b101061l
68. Gil, M. I.; Tomás-Barberán, F. A.; Hess-Pierce, B.; Holcroft, D. M.; Kader, A. A. Antioxidant activity of pomegranate juice and its relationship with phenolic composition and processing J. Agric. Food Chem. 2000, 48, 4581-4589 10.1021/jf000404a
69. Seeram, N. P.; Adams, L. S.; Henning, S. M.; Niu, Y.; Zhang, Y.; Nair, M. G.; Heber, D. In vitro antiproliferative, apoptotic and antioxidant activities of punicalagin, ellagic acid and a total pomegranate tannin extract are enhanced in combination with other polyphenols as found in pomegranate juice J. Nutr. Biochem. 2005, 16, 360-367 10.1016/j.jnutbio.2005.01.006
70. Tanaka, T.; Nonaka, G.; Nishika, I. Tannins and related compounds XL. Revision of the structures of punicalin and punicalagin, and isolation and characterization of 2-O-galloylpunicalin from the bark of Punica granatum L Chem. Pharm. Bull. 1986, 34, 650-655 10.1248/cpb.34.650
71. Lu, J.; Ding, K.; Yuan, Q. Determination of punicalagin isomers in pomegranate husk Chromatographia 2008, 68, 303-306 10.1365/s10337-008-0699-y
72. Tanaka, T.; Nonaka, G.; Nishika, I. Tannins and related compounds XLI. Isolation and characterization of novel ellagitannins, punicacorteins A, B, C and D, and punigluconin from the bark of Punica granatum L Chem. Pharm. Bull. 1986, 34, 656-663 10.1248/cpb.34.656
73. Cai, Y. Z.; Xing, J.; Sun, M.; Zhan, Z. Q.; Corke, H. Phenolic antioxidants (hydrolyzable tannins, flavonols, and anthocyanins) identified by LC-ESI-MS and MALDI-QIT-TOF MS from Rosa chinensis flowers J. Agric. Food Chem. 2005, 53, 9940-9948 10.1021/jf052137k
74. Gu, L.; Kelm, M. A.; Hammerstone, J. F.; Zhang, Z.; Beecher, G.; Holden, J.; Haytowitz, D.; Prior, R. L. Liquid chromatographic/electrospray ionization mass spectrometric studies of proanthocyanidins in foods J. Mass Spectrom. 2003, 38, 1272-1280 10.1002/jms.541
75. Esatbeyoglu, T.; Wray, V.; Winterhalter, P. Identification of two novel prodelphinidin A-type dimers from roasted hazelnut skins (Corylus avellana L.) J. Agric. Food Chem. 2013, 61, 12640-12645 10.1021/jf404549w
76. Bresciani, L.; Calani, L.; Cossu, M.; Mena, P.; Sayegh, M.; Ray, S.; Del Rio, D. (Poly)phenolic characterization of three food supplements containing 36 different fruits, vegetables and berries PharmaNutrition 2015, 3, 11-19 10.1016/j.phanu.2015.01.001
77. Huang, Y.; Chen, L.; Feng, L.; Guo, F.; Li, Y. Characterization of total phenolic constituents from the stems of Spatholobus suberectus using LC-DAD-MSn and their inhibitory effect on human neutrophil elastase activity Molecules 2013, 18, 7549-7556 10.3390/molecules18077549
78. Yoshimura, Y.; Zaima, N.; Moriyama, T.; Kawamura, Y. Different localization patterns of anthocyanin species in the pericarp of black rice revealed by imaging mass spectrometry PLoS One 2012, 7, e31285 10.1371/journal.pone.0031285
79. Gómez-Caravaca, A. M.; Verardo, V.; Toselli, M.; Segura-Carretero, A.; Fernández-Gutiérrez, A.; Caboni, M. F. Determination of the major phenolic compounds in pomegranate juices by HPLC-DAD-ESI-MS J. Agric. Food Chem. 2013, 61, 5328-5337 10.1021/jf400684n
80. Du, C. T.; Wang, P. L.; Francis, F. J. Anthocyanins of pomegranate J. Food Sci. 1975, 40, 417-418 10.1111/j.1365-2621.1975.tb02217.x