Comparative Analysis of Phenolic Content and Profile, Antioxidant Capacity, and Anti-inflammatory Bioactivity in Wild Alaskan and Commercial Vaccinium Berries
Abstract

Wild Alaskan Vaccinium berries, V. vitis-idaea (lowbush cranberry) and V. uliginosum (bog blueberry), were investigated in parallel with their commercial berry counterparts, V. macrocarpon (cranberry) and V. angustifolium (lowbush blueberry). Lowbush cranberry accumulated about twice the total phenolics (624.4 mg/100 g FW) and proanthocyanidins (278.8 mg/100 g) content as commercial cranberries, but A-type proanthocyanidins were more prevalent in the latter. Bog blueberry anthocyanin and total phenolic contents of 220 and 504.5 mg/100 g, respectively, significantly exceeded those of the lowbush blueberry. Chlorogenic acid, however, was quite high in lowbush blueberry (83.1 mg/100 g), but undetected in bog blueberry, and the proanthocyanidins of lowbush blueberry had significantly higher levels of polymerization. Antioxidant capacity (DPPH, APTS, and FRAP) correlated with phenolic content for each berry. A polyphenol-rich fraction from lowbush cranberry exhibited dose-dependent inhibition of LPS-elicited induction of IL-1β in RAW 264.7 cells, indicative of strong anti-inflammatory activity. These results corroborate the historic use of wild Alaskan berries as medicinally important foods in Alaska Native communities.
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- Samir C. Debnath, Juran C. Goyali. In Vitro Propagation and Variation of Antioxidant Properties in Micropropagated Vaccinium Berry Plants—A Review. Molecules 2020, 25 (4) , 788. https://doi.org/10.3390/molecules25040788
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- Kamila Hurkova, Leos Uttl, Josep Rubert, Klara Navratilova, Vladimir Kocourek, Milena Stranska-Zachariasova, Frantisek Paprstein, Jana Hajslova. Cranberries versus lingonberries: A challenging authentication of similar Vaccinium fruit. Food Chemistry 2019, 284 , 162-170. https://doi.org/10.1016/j.foodchem.2019.01.014
- Mary H. Grace, Jia Xiong, Debora Esposito, Mark Ehlenfeldt, Mary Ann Lila. Simultaneous LC-MS quantification of anthocyanins and non-anthocyanin phenolics from blueberries with widely divergent profiles and biological activities. Food Chemistry 2019, 277 , 336-346. https://doi.org/10.1016/j.foodchem.2018.10.101
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- José M. Lorenzo, Mario Estévez, Francisco J. Barba, Rohit Thirumdas, Daniel Franco, Paulo Eduardo Sichetti Munekata. Polyphenols: Bioaccessibility and bioavailability of bioactive components. 2019,,, 309-332. https://doi.org/10.1016/B978-0-12-814174-8.00011-1
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- Cara K. Isaak, Jay C. Petkau, Heather Blewett, Karmin O, Yaw L. Siow. Lingonberry anthocyanins protect cardiac cells from oxidative-stress-induced apoptosis. Canadian Journal of Physiology and Pharmacology 2017, 95 (8) , 904-910. https://doi.org/10.1139/cjpp-2016-0667
- Erdal YABALAK, AHMET MURAT GİZİR. Evaluation of Total Polyphenol Content, Antioxidant Activity and Chemical Composition of Methanolic Extract from Allium Kharputense Freyn et. Sint. and Determination of Mineral and Trace Elements. Journal of the Turkish Chemical Society, Section A: Chemistry 2017, , 691-691. https://doi.org/10.18596/jotcsa.315094
- Michael A. Timmers, Mary H. Grace, Gad G. Yousef, Mary Ann Lila. Inter- and intra-seasonal changes in anthocyanin accumulation and global metabolite profiling of six blueberry genotypes. Journal of Food Composition and Analysis 2017, 59 , 105-110. https://doi.org/10.1016/j.jfca.2017.02.019
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- Cheng-Yong Feng, Wei-Wei Wang, Jian-Fei Ye, Shan-Shan Li, Qian Wu, Dan-Dan Yin, Bing Li, Yan-Jun Xu, Liang-Sheng Wang. Polyphenol profile and antioxidant activity of the fruit and leaf of Vaccinium glaucoalbum from the Tibetan Himalayas. Food Chemistry 2017, 219 , 490-495. https://doi.org/10.1016/j.foodchem.2016.09.083
- Nathalie J. Plundrich, Rishipal R. Bansode, E. Allen Foegeding, Leonard L. Williams, Mary Ann Lila. Protein-bound Vaccinium fruit polyphenols decrease IgE binding to peanut allergens and RBL-2H3 mast cell degranulation in vitro. Food & Function 2017, 8 (4) , 1611-1621. https://doi.org/10.1039/C7FO00249A
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- Chengyong Feng, Shang Su, Lijin Wang, Jie Wu, Zhongqiu Tang, Yanjun Xu, Qingyan Shu, Liangsheng Wang. Antioxidant capacities and anthocyanin characteristics of the black–red wild berries obtained in Northeast China. Food Chemistry 2016, 204 , 150-158. https://doi.org/10.1016/j.foodchem.2016.02.122
- Ya Li, Jiao-Jiao Zhang, Dong-Ping Xu, Tong Zhou, Yue Zhou, Sha Li, Hua-Bin Li. Bioactivities and Health Benefits of Wild Fruits. International Journal of Molecular Sciences 2016, 17 (8) , 1258. https://doi.org/10.3390/ijms17081258
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- Stéphanie Dudonné, Pascal Dubé, Fernando Forato Anhê, Geneviève Pilon, André Marette, Mélanie Lemire, Cory Harris, Eric Dewailly, Yves Desjardins. Comprehensive analysis of phenolic compounds and abscisic acid profiles of twelve native Canadian berries. Journal of Food Composition and Analysis 2015, 44 , 214-224. https://doi.org/10.1016/j.jfca.2015.09.003
- Ruisong Pei, Mo Yu, Richard Bruno, Bradley W. Bolling. Phenolic and tocopherol content of autumn olive (Elaeagnus umbellate) berries. Journal of Functional Foods 2015, 16 , 305-314. https://doi.org/10.1016/j.jff.2015.04.028
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