Exploring the Bioactive Potential of Cistus ladanifer Leaves from Northern Morocco (Tangier)

• Autorzy: Abdelfattah Bahia , Mrabet Amena , Simou Ayoub , Khaddor Mohamed

Identyfikatory

DOI

10.12912/27197050/187764

• Języki publikacji: EN

Abstrakty

EN

The present research explored the antioxidant capacities and phytochemical profile of Cistus ladanifer collected from North Morocco (Tangier), to identify potential medicinal sources of antioxidants. The antioxidant qualities of the extracts were assessed using a variety of analytical methods, such as 2,2-Diphenyl-1-picrylhydrazyl (DPPH), ferric reducing antioxidant power (FRAP), 2,2’-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS), and oxygen radical absorbance capacity (ORAC). Fourier transform infrared (FTIR) spectroscopy, gas chromatography-mass spectrometry (GC-MS), and high-performance liquid chromatography (HPLC) were employed to examine the chemical constituents present in the plant material. Finally, ICP-AES analysis was performed to characterize the nutritional components of the extract, providing detailed insights into its valuable nutrient content. The findings revealed that the methanolic extract displayed considerable antioxidant potential, as evidenced by its powerful scavenging activities against DPPH, with an IC₅₀ value of 0.115 ± 0.003 mg/ml and IC₅₀ of 0.251 ± 0.006 mg/ml ABTS radicals. Moreover, it displayed a higher reducing power using the FRAP test and excellent ORAC values, with 62.74 ± 0.07 mg/g and 40.21 ± 0.7 mg/g dry weight of extract, respectively. This research also assessed the total phenolic and total flavonoid compounds, while tannins were found in high concentrations in the methanolic extract, with 69.08 ± 1.69 mg of GAE/g dW, 47.86 ± 1.76 mg of QE/g dW, and 354.98 ± 15.29 mg of TAE/g dW, respectively. The presence of phenols, benzene rings, aromatic compounds, ethers, and methylene chains was verified by FTIR analysis. Finally, HPLC-MS and GC-MS analyses revealed a rich profile of bioactive phytochemicals. This study is the first of its kind to be conducted in Tangier, Northern Morocco, shedding light on the unique chemical composition of Cistus ladanifer in this region.

Słowa kluczowe

EN

antioxidant capacities; chemical composition; Cistus ladanifer; natural sources; Nutritional components; phytochemicals; Tangier

• Wydawca: Lubelski Oddział Polskiego Towarzystwo Inżynierii Ekologicznej ; Lublin University of Technology ; WNGB Wydawnictwo Naukowe
• Czasopismo: Ecological Engineering & Environmental Technology
• Rocznik: 2024
• Tom: Vol. 25, iss. 6
• Strony: 316--330
• Opis fizyczny: Bibliogr. 64 poz., rys., tab.

Twórcy

autor

Abdelfattah Bahia

• Laboratory of Materials, Natural Substances and Environment (LAMSE), Chemistry Department, Faculty of Sciences and Techniques of Tangier, P.O. Box 416, Tangier 90000, Morocco

• https://orcid.org/0009-0008-8311-2513

autor

Mrabet Amena

• Laboratory of Materials, Natural Substances and Environment (LAMSE), Chemistry Department, Faculty of Sciences and Techniques of Tangier, P.O. Box 416, Tangier 90000, Morocco

• https://orcid.org/0009-0004-3709-2997

autor

Simou Ayoub

• Laboratory of Materials, Natural Substances and Environment (LAMSE), Chemistry Department, Faculty of Sciences and Techniques of Tangier, P.O. Box 416, Tangier 90000, Morocco

• https://orcid.org/0009-0002-2314-3541

autor

Khaddor Mohamed

• Laboratory of Materials, Natural Substances and Environment (LAMSE), Chemistry Department, Faculty of Sciences and Techniques of Tangier, P.O. Box 416, Tangier 90000, Morocco

• https://orcid.org/0000-0002-0461-5462

Bibliografia

• 1. Altemimi, A., Lakhssassi, N., Baharlouei, A., Watson, D., Lightfoot, D. 2017. Phytochemicals: extraction, isolation, and identification of bioactive compounds from plant extracts. Plants, 6(4), 42. https://doi.org/10.3390/plants6040042
• 2. Amensour, M., Sendra, E., Pérez-Alvarez, J.A., Skali-Senhaji, N., Abrini, J., Fernández-López, J. 2010. Antioxidant activity and chemical content of methanol and ethanol extracts from leaves of rockrose (Cistus ladaniferus). Plant Foods for Human Nutrition, 65(2), 170–178. https://doi.org/10.1007/s11130-010-0168-2
• 3. Arroussi, J., Ouerfelli, M., Smaoui, A., Ahmed, H.B., Kaâb, S.B., Kaâb, L.B.B. 2022. Antioxidant activity of seven plant extracts collected from Tunisia and their allelopathic potential on Lactuca sativa L. and Phalaris minor L. South African Journal of Botany, 148, 135– 143. https://doi.org/10.1016/j.sajb.2022.04.029
• 4. Bai, J., Wu, Y., Bu, Q., Zhong, K., Gao, H. 2022. Comparative study on antibacterial mechanism of shikimic acid and quinic acid against Staphylococcus aureus through transcriptomic and metabolomic approaches. LWT, 153, 112441. https://doi.org/10.1016/j.lwt.2021.112441
• 5. Bakrim, H., Zerrouk, M.H., Galiou, O.E., Attaleb, M., Benbacer, L., Mzibri, M.E., Laglaoui, A. 2021. Bioactive properties of natural compounds extracted from leaves of Cistus ladanifer. Ecology, Environment and Conservation Journal, 27(4), (1563–1574)
• 6. Barrajón-Catalán, E., Fernández-Arroyo, S., Roldán, C., Guillén, E., Saura, D., Segura-Carretero, A., Micol, V. 2011. A systematic study of the polyphenolic composition of aqueous extracts deriving from several Cistus genus species: evolutionary relationship: polyphenolic characterization of Cistus Aqueous Extracts. Phytochemical Analysis, 22(4), 303–312. https://doi.org/10.1002/pca.1281
• 7. Barrajón-Catalán, E., Fernández-Arroyo, S., Saura, D., Guillén, E., Fernández-Gutiérrez, A., Segura-Carretero, A., Micol, V. 2010. Cistaceae aqueous extracts containing ellagitannins show antioxidant and antimicrobial capacity, and cytotoxic activity against human cancer cells. Food and Chemical Toxicology, 48(8–9), 2273–2282. https://doi.org/10.1016/j.fct.2010.05.060
• 8. Barros, J.A.V.A., De Souza, P.F., Schiavo, D., Nóbrega, J.A. 2016. Microwave-assisted digestion using diluted acid and base solutions for plant analysis by ICP OES. Journal of Analytical Atomic Spectrometry, 31(1), 337–343. https://doi.org/10.1039/C5JA00294J
• 9. Benali, T., Bouyahya, A., Habbadi, K., Zengin, G., Khabbach, A., Achbani, E. H., Hammani, K. 2020. Chemical composition and antibacterial activity of the essential oil and extracts of Cistus ladaniferus subsp. ladanifer and Mentha suaveolens against phytopathogenic bacteria and their ecofriendly management of phytopathogenic bacteria. Biocatalysis and Agricultural Biotechnology, 28, 101696. https://doi.org/10.1016/j.bcab.2020.101696
• 10. Benyahya, H., Mohti, H., Rhaffari, L.E., Zaid, A. 2023. Qualitative and quantitative ethnobotanical analysis of the knowledge of indigenous populations on medicinal plants in the Meknes region of Morocco. Universal Journal of Plant Science, 10(1), 1–25. https://doi.org/10.13189/ujps.2023.100101
• 11. Blois, M.S. 1958. Antioxidant determinations by the use of a stable free radical. Nature, 181(4617), 1199–1200. https://doi.org/10.1038/1811199a0
• 12. Bouothmany, K., Bourhia, M., Aoussar, N., Attaleb, M., Salamatullah, A., Nafidi, H.A., Benbacer, L. 2022. Leaf extracts of Cistus ladanifer exhibit potent antioxidant and antiproliferative activities against liver, prostate and breast cancer cells. Applied Sciences, 12(17), 8603. https://doi.org/10.3390/app12178603
• 13. Bunaciu, A.A., Aboul-Enein, H.Y., Fleschin, S. 2010. Application of fourier transform infrared spectrophotometry in pharmaceutical drugs analysis. Applied Spectroscopy Reviews, 45(3), 206–219. https://doi.org/10.1080/00387011003601044
• 14. Ceci, C., Lacal, P.M., Tentori, L., De Martino, M.G., Miano, R., Graziani, G. 2018. Experimental evidence of the antitumor, antimetastatic and antiangiogenic activity of ellagic acid. Nutrients, 10(11), 1756. https://doi.org/10.3390/nu10111756
• 15. Ci, K.C., Indira G. 2016. Quantitative estimation of total phenolic, flavonoids, tannin and chlorophyll content of leaves of Strobilanthes Kunthiana (Neelakurinji).Journal of Medicinal Plants Studies,
• 16. Dar, R.A., Shahnawaz, M., Ahanger, M.A., Majid, I.U. 2023. Exploring the diverse bioactive compounds from medicinal plants: A Review. The Journal of Phytopharmacology, 12(3), 189–195. https://doi.org/10.31254/phyto.2023.12307
• 17. Drava, G., Minganti, V. 2020. Influence of an internal standard in axial ICP OES analysis of trace elements in plant materials. Journal of Analytical Atomic Spectrometry, 35(2), 301–306. https://doi.org/10.1039/C9JA00372J
• 18. El Hamsas El Youbi, A., El Mansouri, L., Boukhira, S., Daoudi, A., Bousta, D. 2016. In vivo anti-inflammatory and analgesic effects of aqueous extract of Cistus ladanifer L. from Morocco. American Journal of Therapeutics, 23(6), e1554–e1559. https://doi.org/10.1097/MJT.0000000000000419
• 19. El Karkouri, J., Bouhrim, M., Al Kamaly, O.M., Mechchate, H., Kchibale, A., Adadi, I., Amine, S., Alaoui Ismaili, S., Zair, T. 2021. Chemical composition, antibacterial and antifungal activity of the essential oil from Cistus ladanifer L. Plants, 10(10), 2068. https://doi.org/10.3390/plants10102068
• 20. Ennoury, A., BenMrid, R., Nhhala, N., Roussi, Z., Latique, S., Zouaoui, Z., Nhiri, M. 2022. River’s Ulva intestinalis extract protects common bean plants (Phaseolus vulgaris L.) against salt stress. South African Journal of Botany, 150, 334–341. https://doi.org/10.1016/j.sajb.2022.07.035
• 21. Ennoury, A., Roussi, Nhhala Z., Zouaoui, Z., Kabach, I., Krid, A., Kchikich, A., Nhiri, M. 2022. Effect of atriplex halimus extract as a biostimulant on physiological and biochemical regulation in faba bean plants. (Preprint). https://doi.org/10.21203/rs.3.rs-1773923/v1
• 22. Ercan, L., Doğru, M. 2022. Antioxidant and antimicrobial capacity of quinic acid. Bitlis Eren Üniversitesi Fen Bilimleri Dergisi, 11(4), 1018–1025. https://doi.org/10.17798/bitlisfen.1167047
• 23. Escribano, J., Cabanes, J., Jiménez-Atiénzar, M., Ibañez-Tremolada, M., Gómez-Pando, L. R., García-Carmona, F., Gandía-Herrero, F. 2017. Characterization of betalains, saponins and antioxidant power in differently colored quinoa (Chenopodium quinoa) varieties. Food Chemistry, 234, 285–294. https://doi.org/10.1016/j.foodchem.2017.04.187
• 24. Gallego, M. G., Gordon, M. H., Segovia, F. J., Skowyra, M., Almajano, M. P. 2013. Antioxidant properties of three aromatic herbs (rosemary, thyme and lavender) in oil-in-water emulsions. Journal of the American Oil Chemists’ Society, 90(10), 1559– 1568. https://doi.org/10.1007/s11746-013-2303-3
• 25. Gaweł-Bęben, K., Kukula-Koch, W., Hoian, U., Czop, M., Strzępek-Gomółka, M., Antosiewicz, B. 2020. Characterization of Cistus × incanus L. and Cistus ladanifer L. Extracts as potential multifunctional antioxidant ingredients for skin protecting cosmetics. Antioxidants, 9(3), 202. https://doi.org/10.3390/antiox9030202
• 26. Vaisnav G., Chakraborty A.K., Karole S. 2023. Design, synthesis and evaluation of some novel derivatives of cinnamic acid as anti-inflammatory agents. World Journal of Biology Pharmacy and Health Sciences, 14(1), 088–096. https://doi.org/10.30574/wjbphs.2023.14.1.0164
• 27. Glevitzky, I., Dumitrel, G.A., Glevitzky, M., Pasca, B., Otrisal, P., Bungau, S., Cioca, G., Pantis, C., and Popa, M. 2019. Statistical analysis of the relationship between antioxidant activity and the structure of flavonoid compounds. Revista de Chimie, 70(9), 3103–3107. https://doi.org/10.37358/RC.19.9.7497
• 28. Guimarães, R., Sousa, M.J., Ferreira, I.C.F.R. 2010. Contribution of essential oils and phenolics to the antioxidant properties of aromatic plants. Industrial Crops and Products, 32(2), 152–156. https://doi.org/10.1016/j.indcrop.2010.04.011
• 29. Gülçın, İ., Oktay, M., Kıreçcı, E., Küfrevıoǧlu, Ö.İ. 2003. Screening of antioxidant and antimicrobial activities of anise (Pimpinella anisum L.) seed extracts. Food Chemistry, 83(3), 371–382. https://doi.org/10.1016/S0308-8146(03)00098-0
• 30. Zidane H., Elmiz M., Aouinti F., Tahani A., Wathelet J., Sindic M., Elbachiri A. 2013. Chemical composition and antioxidant activity of essential oil, various organic extracts of Cistus ladanifer and Cistus libanotis growing in Eastern Morocco. African Journal of Biotechnology, 12(34), 5314–5320. https://doi.org/10.5897/AJB2013.12868
• 31. Huang, Z., Kuang, J., Yu, M., Ding, D. 2023. Quinic acid as a novel depressant for efficient flotation separation of scheelite from calcite. Physicochemical Problems of Mineral Processing. https://doi.org/10.37190/ppmp/166008
• 32. Ibragic, S., Barbini, S., Oberlerchner, J.T., Potthast, A., Rosenau, T., Böhmdorfer, S. 2021. Antioxidant properties and qualitative analysis of phenolic constituents in Ephedra spp. by HPTLC together with injection port derivatization GC–MS. Journal of Chromatography B, 1180, 122877. https://doi.org/10.1016/j.jchromb.2021.122877
• 33.Jiang, Y., Li, H., Li, P., Cai, Z., Ye, W. 2005. Steroidal alkaloids from the bulbs of Fritillaria p uqiensis. Journal of Natural Products, 68(2), 264–267. https://doi.org/10.1021/np0497649
• 34. Kachmar, M.R., Naceiri Mrabti, H., Bellahmar, M., Ouahbi, A., Haloui, Z., El Badaoui, K., Bouyahya, A., Chakir, S. 2021. Traditional knowledge of medicinal plants used in the northeastern part of Morocco. Evidence-Based Complementary and Alternative Medicine, 2021, e6002949. https://doi.org/10.1155/2021/6002949
• 35. Khade, O.S.K., Sonkar, R.M., Gade, P.S., Bhatt, P. 2023. Plant secondary metabolites: extraction, screening, analysis and their bioactivity. International Journal of Herbal Medicine, 11(2), 01–17. https://doi.org/10.22271/flora.2023.v11.i2a.855
• 36. Kosani, M., Manojlovi, N. 2014. Biological activities and chemical composition of lichens from Serbia. EXCLI Journal, 13, 1226–1238.
• 37. Kumar, V., Sharma, A., Bhardwaj, R., Thukral, A.K. 2019. Elemental Composition of plants and multivariate analysis. National Academy Science Letters, 42(1), 45–50. https://doi.org/10.1007/s40009-018-0715-1
• 38. Lemhadri, A., Achtak, H., Lamraouhi, A., Louidani, N., Benali, T., Dahbi, A., Bouyahya A., Khouchlaa A.,Ali Shariati A., Hano Ch, Lorenzo J.M. , Chen J.T., Lyoussi, B. 2023. Diversity of medicinal plants used by the local communities of the coastal plateau of safi province (Morocco). Frontiers in Bioscience-Scholar, 15(1), 1. https://doi.org/10.31083/j.fbs1501001
• 39. Liu, W., Cui, X., Zhong, Y., Ma, R., Liu, B., Xia, Y. 2023. Phenolic metabolites as therapeutic in inflammation and neoplasms: molecular pathways explaining their efficacy. Pharmacological Research, 193, 106812. https://doi.org/10.1016/j.phrs.2023.106812
• 40. Luyindula, Z.N. 2017. Carence en oligoéléments en relation avec la croissance, la production etla composition minérale du haricot en milieu contrôlé. International Journal of Biological and Chemical Sciences, 11(3), 1075. https://doi.org/10.4314/ijbcs.v11i3.12
• 41. Mendes, M., Carvalho, A.P., Magalhães, J.M.C.S., Moreira, M., Guido, L., Gomes, A.M., Delerue-Matos, C. 2016. Response surface evaluation of microwave-assisted extraction conditions for Lycium barbarum bioactive compounds. Innovative Food Science & Emerging Technologies, 33, 319–326. https://doi.org/10.1016/j.ifset.2015.12.025
• 42. Merrouni, I.A., Kharchoufa, L., Bencheikh, N., Elachouri, M. 2021. Ethnobotanical profile of medicinal plants used by people of north-eastern Morocco: cross-cultural and historical approach (Part I). Ethnobotany Research and Applications, 21, 1–45.
• 43. Muazu M., Sani A.M., Dikwa K.B., Dibal D.M. 2022. GC-MS Analysis and antiplasmodial potentials of bioactive compounds present in methanolic and ethanolic leaf extracts of Daniella oliveri. Asian Journal of Biochemistry, Genetics and Molecular Biology, 26–34. https://doi.org/10.9734/ajbgmb/2022/v12i130284
• 44. Nsofor, W.N., Nwaoguikpe, R.N., Ujowundu, F.N., Keke, C O., Uba, M.T., Edom, C.V. 2023. Phytochemical, GC-MS, FTIR and amino acid profile of methanol extract of Tetrapleura tetraptera fruit. Journal of Drug Delivery and Therapeutics, 13(2), 61–69. https://doi.org/10.22270/jddt.v13i2.5739
• 45. Olszowy-Tomczyk, M., Wianowska, D. 2023. Antioxidant properties of selected flavonoids in binary mixtures—considerations on myricetin, kaempferol and quercetin. International Journal of Molecular Sciences, 24(12), 10070. https://doi.org/10.3390/ijms241210070
• 46. Poonguzhali, E., Dalmia, M., Sofiya, K., Kapoor, A., Prabhakar, S. 2023. Separation of phenol through solvent extraction from aqueous solutions. AIP Conference Proceedings, 2427(1), 020083. https://doi.org/10.1063/5.0101070
• 47. Priyanka Singh, Gupta, E., Neha Mishra, and Mishra, P. 2020. Shikimic acid as intermediary model for the production of drugs effective against influenza virus. In Phytochemicals as Lead Compounds for New Drug Discovery (pp. 245–256). https://doi.org/10.1016/B978-0-12-817890-4.00016-0
• 48.Raimundo, J.R., Frazão, D.F., Domingues, J.L., Quintela-Sabarís, C., Dentinho, T.P., Anjos, O., Alves, M., Delgado, F. 2018. Neglected mediterranean plant species are valuable resources: the example of Cistus ladanifer. Planta, 248(6), 1351–1364. https://doi.org/10.1007/s00425-018-2997-4
• 49. Ramya, S., Loganathan, T., Chandran, M., Priyanka, R., Kavipriya, K., Grace Lydial Pushpalatha, G., Saluja, V. 2022. Phytochemical Screening, GCMS, FTIR profile of Bioactive Natural Products in the methanolic extracts of Cuminum cyminum seeds and oil. Journal of Drug Delivery and Therapeutics, 12(2-S), 110–118. https://doi.org/10.22270/jddt.v12i2-S.5280
• 50. Saadullah, M., Asif, M., Sattar, A., Rehman, K., Shah, S., Saleem, M., Afzal, K. 2020. Cytotoxic and antioxidant potentials of ellagic acid derivatives from Conocarpus lancifolius (Combretaceae). Tropical Journal of Pharmaceutical Research, 19(5), 1037–1080. https://doi.org/10.4314/tjpr.v19i5.24
• 51. Saur, E. 1990. Mise au point bibliographique, au sujet de la nutrition oligo-minérale des plantes supérieures. Carences et toxicités chez les conifères. Annales des Sciences Forestières, 47(4), 367–389. https://doi.org/10.1051/forest:19900408
• 52. Sayah, K., Marmouzi, I., Naceiri Mrabti, H., Cherrah, Y., Faouzi, M.E.A. 2017. Antioxidant activity and inhibitory potential of Cistus salviifolius L. and Cistus monspeliensis L. Aerial parts extracts against key enzymes linked to hyperglycemia. BioMed Research International, 2017, 1–7. https:// doi.org/10.1155/2017/2789482
• 53. Sebastiani, G., Almeida-Toledano, L., Serra-Delgado, M., Navarro-Tapia, E., Sailer, S., Valverde, O., Garcia-Algar, O., and Andreu-Fernández, V. 2021. Therapeutic effects of catechins in less common neurological and neurodegenerative disorders. Nutrients, 13(7), 2232. https://doi.org/10.3390/nu13072232
• 54. Serbouti, S., Ettaqy, A., Boukcim, H., Mderssa, M.E., El Ghachtouli, N., Abbas, Y. 2023. Forests and woodlands in Morocco: review of historical evolution, services, priorities for conservation measures and future research. International Forestry Review, 25(1), 121–145. https://doi.org/10.1505/146554823836838745
• 55. Shahidi, F., Zhong, Y. 2010. Novel antioxidants in food quality preservation and health promotion. European Journal of Lipid Science and Technology, 112(9), 930–940. https://doi.org/10.1002/ejlt.201000044
• 56. Spigno, G., Tramelli, L., De Faveri, D.M. 2007. Effects of extraction time, temperature and solvent on concentration and antioxidant activity of grape marc phenolics. Journal of Food Engineering, 81(1), 200–208. https://doi.org/10.1016/j.jfoodeng.2006.10.021
• 57. Sutariya, S., Ahmad Shah, A., Bajpai, A., Sharma, R.J., Pandhurnekar, C.P., Gupta, A. 2023. Fourier transform infrared spectroscopy (FTIR) analysis, antioxidant and anti-inflammatory activities of leaf and fruit extracts of Gymnosporia montana. Materials Today: Proceedings, 73, 134–141. https://doi.org/10.1016/j.matpr.2022.09.462
• 58.Bobrysheva T.N. 2023. Polyphenols as promising bioactive compounds. Voprosy Pitaniya, 92 1(1), 92–107. https://doi.org/10.33029/0042-8833-2023-92-1-92-107
• 59. Ulpathakumbura et al. 2023. FTIR spectral correlation with alpha-glucosidase inhibitory activities of selected leafy plants extracts. International Journal of Plant Based Pharmaceuticals, 3(3), 104–113. https://doi.org/10.29228/ijpbp.22
• 60. Valko, M., Leibfritz, D., Moncol, J., Cronin, M.T.D., Mazur, M., Telser, J. 2007. Free radicals and antioxidants in normal physiological functions and human disease. The International Journal of Biochemistry & Cell Biology, 39(1), 44–84. https://doi.org/10.1016/j.biocel.2006.07.001
• 61. Wen, L., Wu, D., Tan, X., Zhong, M., Xing, J., Li, W., Li, D., Cao, F. 2022. The role of catechins in regulating diabetes: an update review. Nutrients, 14(21), 4681. https://doi.org/10.3390/nu14214681
• 62. Yoon, J.H., Kim, M.Y., Cho, J.Y. 2023. Apigenin: a therapeutic agent for treatment of skin inflammatory diseases and cancer. International Journal of Molecular Sciences, 24(2), 1498. https://doi.org/10.3390/ijms24021498
• 63. Yunitasari, N., Swasono, R.T., Pranowo, H.D., Raharjo, T.J. 2022. Phytochemical screening and metabolomic approach based on Fourier transform infrared (FTIR): identification of α-amylase inhibitor metabolites in Vernonia amygdalina leaves. Journal of Saudi Chemical Society, 26(6), 101540. https://doi.org/10.1016/j.jscs.2022.101540
• 64. Zulueta, A., Esteve, M.J., Frígola, A. 2009. ORAC and TEAC assays comparison to measure the antioxidant capacity of food products. Food Chemistry, 114(1), 310–316. https://doi.org/10.1016/j.foodchem.2008.09.033