Unlocking Quercetin's Neuroprotective Potential: A Focus on Bee-Collected Pollen
Corresponding Author
Aleksandar Ž. Kostić
Chair of Chemistry and Biochemistry, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Belgrade
Search for more papers by this authorDılhun Keriman Arserim-Uçar
Department of Nutrition and Dietetics, Faculty of Health Sciences, Bingöl University, Bingöl, 12000 Türkiye
Search for more papers by this authorMałgorzata Materska
Department of Chemistry, Faculty of Food Science and Biotechnology, University of Life Sciences in Lublin, Akademicka 15 Street, 20-950 Lublin, Poland
Search for more papers by this authorBarbara Sawicka
Department of Plant Production Technology and Commodities Science, University of Life Sciences in Lublin, 20-950 Lublin, Poland
Search for more papers by this authorDominika Skiba
Department of Plant Production Technology and Commodities Science, University of Life Sciences in Lublin, 20-950 Lublin, Poland
Search for more papers by this authorDanijel D. Milinčić
Chair of Chemistry and Biochemistry, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Belgrade
Search for more papers by this authorMirjana B. Pešić
Chair of Chemistry and Biochemistry, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Belgrade
Search for more papers by this authorPiotr Pszczółkowski
Experimental Department of Cultivar Assessment, Research Centre for Cultivar Testing, Uhnin, 21-211 Dębowa Kłoda, Poland
Search for more papers by this authorDonya Moradi
Nutrition and Food Sciences Research Center, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran
Search for more papers by this authorParisa Ziarati
Department of Medicinal Chemistry, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran
Search for more papers by this authorBernadetta Bienia
Food Production and Safety Department, National Academy of Applied Sciences, Rynek 1 str., 38-400 Krosno, Poland
Search for more papers by this authorPiotr Barbaś
Department Agronomy of Potato, Plant Breeding and Acclimatization Institute – National Research Institute, Branch Jadwisin, 05-140 Serock, Poland
Search for more papers by this authorMert Sudagıdan
Kit-ARGEM R&D Center, Konya Food and Agriculture University, Meram, 42080 Konya, Türkiye
Search for more papers by this authorPreetinder Kaur
Department of Processing and Food Engineering, College of Agricultural Engineering and Technology, Punjab Agricultural University, Ludhiana, 141004 Punjab
Search for more papers by this authorCorresponding Author
Javad Sharifi-Rad
Facultad de Medicina, Universidad del Azuay, 14-008 Cuenca, Ecuador
Search for more papers by this authorCorresponding Author
Aleksandar Ž. Kostić
Chair of Chemistry and Biochemistry, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Belgrade
Search for more papers by this authorDılhun Keriman Arserim-Uçar
Department of Nutrition and Dietetics, Faculty of Health Sciences, Bingöl University, Bingöl, 12000 Türkiye
Search for more papers by this authorMałgorzata Materska
Department of Chemistry, Faculty of Food Science and Biotechnology, University of Life Sciences in Lublin, Akademicka 15 Street, 20-950 Lublin, Poland
Search for more papers by this authorBarbara Sawicka
Department of Plant Production Technology and Commodities Science, University of Life Sciences in Lublin, 20-950 Lublin, Poland
Search for more papers by this authorDominika Skiba
Department of Plant Production Technology and Commodities Science, University of Life Sciences in Lublin, 20-950 Lublin, Poland
Search for more papers by this authorDanijel D. Milinčić
Chair of Chemistry and Biochemistry, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Belgrade
Search for more papers by this authorMirjana B. Pešić
Chair of Chemistry and Biochemistry, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Belgrade
Search for more papers by this authorPiotr Pszczółkowski
Experimental Department of Cultivar Assessment, Research Centre for Cultivar Testing, Uhnin, 21-211 Dębowa Kłoda, Poland
Search for more papers by this authorDonya Moradi
Nutrition and Food Sciences Research Center, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran
Search for more papers by this authorParisa Ziarati
Department of Medicinal Chemistry, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran
Search for more papers by this authorBernadetta Bienia
Food Production and Safety Department, National Academy of Applied Sciences, Rynek 1 str., 38-400 Krosno, Poland
Search for more papers by this authorPiotr Barbaś
Department Agronomy of Potato, Plant Breeding and Acclimatization Institute – National Research Institute, Branch Jadwisin, 05-140 Serock, Poland
Search for more papers by this authorMert Sudagıdan
Kit-ARGEM R&D Center, Konya Food and Agriculture University, Meram, 42080 Konya, Türkiye
Search for more papers by this authorPreetinder Kaur
Department of Processing and Food Engineering, College of Agricultural Engineering and Technology, Punjab Agricultural University, Ludhiana, 141004 Punjab
Search for more papers by this authorCorresponding Author
Javad Sharifi-Rad
Facultad de Medicina, Universidad del Azuay, 14-008 Cuenca, Ecuador
Search for more papers by this authorAbstract
In the quest to evade side effects associated with synthetic drugs, mankind is continually exploring natural sources. In recent decades, neurodegenerative disorders (NDDs) have surged dramatically compared to other human diseases. Flavonoids, naturally occurring compounds, have emerged as potential preventers of NDD development. Notably, quercetin and its derivatives demonstrated excellent antioxidant properties in the fight against NDDs. Recognizing bee-collected pollen (BP) as a well-established excellent source of quercetin and its derivatives, this review seeks to consolidate available data on the prevalence of this flavonoid in BP, contingent upon its botanical and geographical origins. It aims to advocate for BP as a superb natural source of “drugs” that could serve as preventative measures against NDDs. Examination of numerous published articles, detailing the phenolic profile of BP, suggests that it can be a great source of quercetin, with an average range of up to 1000 mg/kg. In addition to quercetin, 24 derivatives (with rutin being the most predominant) have been identified. Theoretical calculations, based on the recommended dietary intake for quercetin, indicate that BP can fulfil from 0.1 to over 100 % of the requirement, depending on BP's origin and bioaccessibility/bioavailability during digestion.
Graphical Abstract
Conflict of interests
The authors declare no conflict of interest.
Open Research
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
- 1S. A. M. Khalifa, E. H. Elshafiey, A. A. Shetaia, A. A. A. El-Wahed, A. F. Algethami, S. G. Musharraf, M. F. AlAjmi, C. Zhao, S. H. D. Masry, M. M. Abdel-Daim, M. F. Halabi, G. Kai, Y. al Naggar, M. Bishr, M. A. M. Diab, H. R. El-Seedi, Insects 2021, 12, 688.
- 2R. W. Thorp, Plant Syst. Evol. 2000, 222, 211–223.
- 3M. S. Bryś, P. Skowronek, A. Strachecka, Insects 2021, 12, 798.
- 4T. Ischebeck, Biochim. Biophys. Acta (BBA) – Mol. Cell. Biol. Lipid 2016, 1861, 1315–1328.
- 5J. Bertoncelj, T. Polak, T. Pucihar, N. Lilek, A. Kandolf Borovšak, M. Korošec, Int. J. Food Sci. Technol. 2018, 53, 1880–1888.
- 6A. Ž. Kostić, M. B. Pešić, M. D. Mosić, B. P. Dojčinović, M. M. Natić, J. Đ. Trifković, Arch. Industr. Hyg. Toxicol. 2015, 66, 251–258.
- 7I. L. P. de Melo, L. B. de Almeida-Muradian, Quim. Nova 2010, 33, 514–518.
- 8V. A. S. de Arruda, A. A. S. Pereira, A. S. de Freitas, O. M. Barth, L. B. de Almeida-Muradian, J. Food Compos. Anal. 2013, 29, 100–105.
- 9M. Thakur, V. Nanda, Trends Food Sci. Technol. 2020, 98, 82–106.
- 10F. Schulte, J. Mäder, L. W. Kroh, U. Panne, J. Kneipp, Anal. Chem. 2009, 81, 8426–8433.
- 11R. Mărgăoan, L. Al. Mărghitaş, D. S. Dezmirean, F. V. Dulf, A. Bunea, S. A. Socaci, O. Bobiş, J. Agric. Food Chem. 2014, 62, 6306–6316.
- 12C. Y. Salazar-González, F. J. Rodríguez-Pulido, C. M. Stinco, A. Terrab, C. Díaz-Moreno, C. Fuenmayor, F. J. Heredia, Comput. Electron. Agric. 2020, 175, 105601.
- 13S. B. Kim, Q. Liu, J. H. Ahn, Y. H. Jo, A. Turk, I. P. Hong, S. M. Han, B. Y. Hwang, M. K. Lee, Bioorg. Chem. 2018, 81, 127–133.
- 14H. Zhang, R. Liu, Q. Lu, Molecules 2020, 25, 1264.
- 15P. Khongkarat, R. Ramadhan, P. Phuwapraisirisan, C. Chanchao, Heliyon 2020, 6, e03638.
- 16A. Rzepecka-Stojko, J. Stojko, A. Kurek-Górecka, M. Górecki, A. Kabała-Dzik, R. Kubina, A. Moździerz, E. Buszman, Molecules 2015, 20, 21732–21749.
- 17R. Mărgăoan, M. Stranţ, A. Varadi, E. Topal, B. Yücel, M. Cornea-Cipcigan, M. G. Campos, D. C. Vodnar, Antioxidants 2019, 8, 568.
- 18G. Negri, E. W. Teixeira, M. L. T. M. Florêncio Alves, A. C. de C. C. Moreti, I. P. Otsuk, R. G. Borguini, A. Salatino, J. Agric. Food Chem. 2011, 59, 5516–5522.
- 19A. A. M. De-Melo, L. M. Estevinho, M. M. Moreira, C. Delerue-Matos, A. da S. de Freitas, O. M. Barth, L. B. de Almeida-Muradian, J. Food Biochem. 2018, 42, e12536.
- 20A. Ž. Kostić, D. D. Milinčić, U. M. Gašić, N. Nedić, S. P. Stanojević, Ž. Lj. Tešić, M. B. Pešić, LWT-Food Sci. Technol. 2019, 112, 108244.
- 21M. F. Santa Bárbara, M. M. Moreira, C. S. Machado, E. D. Chambó, A. Pascoal, C. A. L. de Carvalho, G. da Silva Sodré, C. Delerue-Matos, L. M. Estevinho, J. Apic. Res. 2021, 60, 99–107.
- 22H. Hemmami, B. ben Seghir, M. ben Ali, A. Rebiai, S. Zeghoud, F. Brahmia, Ovidius Univ. Ann. Chem. 2020, 31, 93–98.
- 23A. Ž. Kostić, D. D. Milinčić, N. Nedić, U. M. Gašić, B. Špirović Trifunović, D. Vojt, Ž. Lj. Tešić, M. B. Pešić, Antioxidants 2021, 10, 1091.
- 24M. Bakour, H. Laaroussi, P. Ferreira-Santos, Z. Genisheva, D. Ousaaid, J. A. Teixeira, B. Lyoussi, Molecules 2022, 27, 5777.
- 25R. Bridi, J. Echeverría, A. Larena, P. Nuñez Pizarro, E. Atala, A. C. de Camargo, W. Y. Oh, F. Shahidi, O. Garcia, K. S. Ah-Hen, G. Montenegro, Front. Pharmacol. 2022, 13, DOI 10.3389/fphar.2022.775219.
- 26F. A. Tomás-Barberán, F. Tomás-Lorente, F. Ferreres, C. Garcia-Viguera, J. Sci. Food Agric. 1989, 47, 337–340.
- 27H. Lv, X. Wang, Y. He, H. Wang, Y. Suo, J. Food Compos. Anal. 2015, 38, 49–54.
- 28G. Negri, L. M. R. C. Barreto, F. L. Sper, C. de Carvalho, M. das G. R. Campos, Braz. J. Food Technol. 2018, 21, DOI 10.1590/1981-6723.17616.
10.1590/1981-6723.17616 Google Scholar
- 29S. Kumar, A. K. Pandey, The Sci. World J. 2013, 2013, 1–16.
- 30K. E. Heim, A. R. Tagliaferro, D. J. Bobilya, J. Nutr. Biochem. 2002, 13, 572–584.
- 31V. Křen, in Glycoscience, Springer Berlin Heidelberg, Berlin, Heidelberg, 2008, pp. 2589–2644.
- 32J. Treml, K. Šmejkal, Compr. Rev. Food Sci. Food Saf. 2016, 15, 720–738.
- 33A. Ž. Kostić, D. D. Milinčić, Ž. Lj. Tešić, M. B. Pešić, in Bee Products and Their Applications in the Food and Pharmaceutical Industries, Elsevier, 2022, pp. 261–282.
- 34M. Symonowicz, M. Kolanek, Biotechnol. Food Sci. 2012, 76, 35–41.
- 35X. Wang, Y. Li, L. Han, J. Li, C. Liu, C. Sun, Front. Cell. Dev. Biol. 2021, 9, 685364.
- 36İ. Gulcin, S. H. Alwasel, Processes 2022, 10, 132.
- 37J. Xiao, Crit. Rev. Food Sci. Nutr. 2015, 55, 1874–1905.
- 38S. Devi, V. Kumar, S. K. Singh, A. K. Dubey, J.-J. Kim, Biomedicine 2021, 9, 99.
- 39A.-S. Michala, A. Pritsa, Diseases 2022, 10, 37.
- 40K. Srinivas, J. W. King, L. R. Howard, J. K. Monrad, J. Food Eng. 2010, 100, 208–218.
- 41W. M. Dabeek, M. V. Marra, Nutrients 2019, 11, 2288.
- 42A. Anand David, R. Arulmoli, S. Parasuraman, Pharmacogn. Rev. 2016, 10, 84.
- 43S. Y. Lee, S. J. Lee, D. G. Yim, S. J. Hur, Foods 2020, 9, 694.
- 44A. Ž. Kostić, D. D. Milinčić, N. S. Stanisavljević, U. M. Gašić, S. Lević, M. O. Kojić, Ž. Lj. Tešić, V. Nedović, M. B. Barać, M. B. Pešić, Food Chem. 2021, 351, 129310.
- 45D. D. Milinčić, N. S. Stanisavljević, A. Ž. Kostić, U. M. Gašić, S. P. Stanojević, Ž. Lj. Tešić, M. B. Pešić, Antioxidants 2022, 11, 2164.
- 46L. Jakobek, Food Chem. 2015, 175, 556–567.
- 47K. Nemeth, M. K. Piskula, Crit. Rev. Food Sci. Nutr. 2007, 47, 397–409.
- 48A. F. Almeida, G. I. A. Borge, M. Piskula, A. Tudose, L. Tudoreanu, K. Valentová, G. Williamson, C. N. Santos, Compr. Rev. Food Sci. Food Saf. 2018, 17, 714–731.
- 49M. Sochocka, B. S. Diniz, J. Leszek, Mol. Neurobiol. 2017, 54, 8071–8089.
- 50H. Khan, H. Ullah, M. Aschner, W. S. Cheang, E. K. Akkol, Biomol. Eng. 2020, 10, 59.
- 51R. B. Maccioni, C. Calfío, A. González, V. Lüttges, Biomol. Eng. 2022, 12, 249.
- 52M. Ciulla, L. Marinelli, I. Cacciatore, A. di Stefano, Biomol. Eng. 2019, 9, 271.
- 53N. Sriraksa, J. Wattanathorn, S. Muchimapura, S. Tiamkao, K. Brown, K. Chaisiwamongkol, Evid.-Based Complement. Altern. Med. 2012, 2012, 1–9.
- 54A. Kumar, N. Sehgal, P. Kumar, S. S. v. Padi, P. S. Naidu, Phytother. Res. 2008, 22, 1563–1569.
- 55Deepika, P. K. Maurya, Molecules 2022, 27, 2498.
- 56A. M. Ares, S. Valverde, J. L. Bernal, M. J. Nozal, J. Bernal, J. Pharm. Biomed. Anal. 2018, 147, 110–124.
- 57Q.-Q. Li, K. Wang, M. C. Marcucci, A. C. H. F. Sawaya, L. Hu, X.-F. Xue, L.-M. Wu, F.-L. Hu, J. Funct. Foods 2018, 49, 472–484.
- 58Y. Zhang, F. Yang, M. Jamali, Z. Peng, Molecules 2016, 21, 1439.
- 59A. Kostić, D. D. Milinčić, B. Špirović Trifunović, N. Nedić, U. M. Gašić, Ž. L. Tešić, S. P. Stanojević, M. B. Pešić, Antioxidants 2023, 12, 1424.
- 60A. Šarić, T. Balog, S. Sobočanec, B. Kušić, V. Šverko, G. Rusak, S. Likić, D. Bubalo, B. Pinto, D. Reali, T. Marotti, Food Chem. Toxicol. 2009, 47, 547–554.
- 61V. Aylanc, A. Tomás, P. Russo-Almeida, S. I. Falcão, M. Vilas-Boas, Antioxidants 2021, 10, 651.
- 62V. Adaškevičiūtė, V. Kaškonienė, K. Barčauskaitė, P. Kaškonas, A. Maruška, Antioxidants 2022, 11, 645.
- 63C.-I. Ilie, E. Oprea, E.-I. Geana, A. Spoiala, M. Buleandra, G. Gradisteanu Pircalabioru, I. A. Badea, D. Ficai, E. Andronescu, A. Ficai, L.-M. Ditu, Antioxidants 2022, 11, 959.
- 64P. Velásquez, G. Montenegro, A. Giordano, M. Retamal, L. M. Valenzuela, CyTA – J. Food 2019, 17, 754–762.
- 65T. Sawicki, M. Ruszkowska, J. Shin, M. Starowicz, Eur. Food Res. Technol. 2022, 248, 2263–2273.
- 66H. Duan, Z. Dong, H. Li, W. Li, S. Shi, Q. Wang, W. Cao, X. Fang, A. Fang, K. Zhai, Food Chem. Toxicol. 2019, 134, 110831.
- 67H. Zhang, Q. Lu, R. Liu, Food Chem. 2022, 375, 131908.
- 68H. Laaroussi, P. Ferreira-Santos, Z. Genisheva, M. Bakour, D. Ousaaid, A. el Ghouizi, J. A. Teixeira, B. Lyoussi, Food Chem. 2023, 405, 134958.
- 69S. Çelik, N. Kutlu, Y. C. Gerçek, S. Bayram, R. Pandiselvam, N. E. Bayram, Foods 2022, 11, 3652.
- 70C. Mutlu, M. Erbas, Food Biosci. 2023, 53, 102805.
- 71C. G. Miguel, O. Anjos, N. B. Sen, E. Guzelmeric, I. Vovk, V. Glavnik, H. Kırmızıbekmez, E. Yesilada, Antioxidants 2023, 12, 1394.
- 72A. C. Gonçalves, R. A. Lahlou, G. Alves, C. Garcia-Viguera, D. A. Moreno, L. R. Silva, Foods 2021, 10, 2804.
- 73M. Oroian, F. Dranca, F. Ursachi, Foods 2022, 11, 2633.
- 74V. Aylanc, S. Ertosun, P. Russo-Almeida, S. I. Falcão, M. Vilas-Boas, Int. J. Food Sci. Technol. 2022, 57, 3490–3502.
- 75N. Ecem Bayram, J. Food Meas. Charact. 2021, 15, 2659–2666.
- 76K. S. Rebelo, C. B. Cazarin, A. H. Iglesias, M. A. Stahl, K. Kristiansen, G. A. Carvalho-Zilse, R. Grimaldi, F. G. Reyes, N. B. Danneskiold-Samsøe, M. R. Júnior, J. Sci. Food Agric. 2021, 101, 4907–4915.
- 77J. E. Oyarzún, M. E. Andia, S. Uribe, P. Núñez Pizarro, G. Núñez, G. Montenegro, R. Bridi, Molecules 2020, 26, 6.
- 78E. Ulusoy, S. Kolayli, J. Food Biochem. 2014, 38, 73–82.
- 79M. G. Campos, C. Frigerio, O. Bobiş, A. C. Urcan, N. G. M. Gomes, Processes 2021, 9, 890.
- 80H. Maruyama, T. Sakamoto, Y. Araki, H. Hara, BMC Complement. Altern. Med. 2010, 10, 30.
- 81N. Almaraz-Abarca, M. da Graça Campos, J. A. Ávila-Reyes, N. Naranjo-Jiménez, J. Herrera Corral, L. S. González-Valdez, J. Food Compos. Anal. 2007, 20, 119–124.
- 82A. Pukalskas, R. Kazernavičiūtė, J. Balžekas, Czech J. Food Sci. 2016, 34, 133–142.
- 83Q. Chu, X. Tian, L. Jiang, J. Ye, J. Agric. Food Chem. 2007, 55, 8864–8869.
- 84M. Thakur, V. Nanda, Food Res. Int. 2021, 140, 110041.
- 85M. Campos, K. R. Markham, K. A. Mitchell, A. P. da Cunha, Phytochem. Anal. 1997, 8, 181–185.
- 86V. Aylanc, S. Larbi, R. Calhelha, L. Barros, F. Rezouga, M. S. Rodríguez-Flores, M. C. Seijo, A. El Ghouizi, B. Lyoussi, S. I. Falcão, M. Vilas-Boas, Molecules 2023, 28, 835.
- 87M. M. Özcan, F. Aljuhaimi, E. E. Babiker, N. Uslu, D. A. Ceylan, K. Ghafoor, M. M. Özcan, N. Dursun, I. M. Ahmed, F. G. Jamiu, O. N. Alsawmahi, J. Apic. Sci. 2019, 63, 69–79.
- 88H. Laaroussi, M. Bakour, D. Ousaaid, A. Aboulghazi, P. Ferreira-Santos, Z. Genisheva, J. A. Teixeira, B. Lyoussi, Food Res. Int. 2020, 138, 109802.
- 89G. Rocchetti, S. Castiglioni, G. Maldarizzi, P. Carloni, L. Lucini, Int. J. Food Sci. Technol. 2019, 54, 335–346.
- 90K. Fatrcová-Šramková, J. Nôžková, M. Máriássyová, M. Kačániová, J. Environ. Sci. Health Part B 2016, 51, 176–181.
- 91A. Ž. Kostić, D. D. Milinčić, M. B. Barać, M. Ali Shariati, Ž. Lj. Tešić, M. B. Pešić, Biomol. Eng. 2020, 10, 84.
- 92V. Aylanc, A. Tomás, P. Russo-Almeida, S. I. Falcão, M. Vilas-Boas, Antioxidants 2021, 10, 651.
- 93H. Ullah, A. di Minno, C. Santarcangelo, A. Tantipongpiradet, M. Dacrema, R. di Matteo, H. R. El-Seedi, S. A. M. Khalifa, A. Baldi, A. Rossi, M. Daglia, Molecules 2022, 27, 9065.
- 94H. Zieliński, W. Wiczkowski, J. Honke, M. K. Piskuła, Antioxidants 2021, 10, 571.
- 95I. Fernández-Jalao, C. Balderas, C. Sánchez-Moreno, B. de Ancos, Innov. Food Sci. Emerg. Technol. 2020, 66, 102486.
- 96M. B. Pešić, D. D. Milinčić, A. Ž. Kostić, N. S. Stanisavljević, G. N. Vukotić, M. O. Kojić, U. M. Gašić, M. B. Barać, S. P. Stanojević, D. A. Popović, N. R. Banjac, Ž. Lj. Tešić, Food Chem. 2019, 284, 28–44.
- 97M. J. Rodríguez-Roque, M. A. Rojas-Graü, P. Elez-Martínez, O. Martín-Belloso, Food Res. Int. 2014, 62, 771–778.