Eritrositlerde Oksidatif Hasara Karşı Arı Ürünlerinin Koruyucu Etkisi
Yıl 2023,
Cilt: 12 Sayı: 1, 167 - 174, 25.03.2023
Orhan Değer
,
Ertuğrul Yiğit
,
Katip Korkmaz
,
Pınar Aygün
,
Ali Asghari
,
Kübra Akbulut Çakıroğlu
,
Selim Demir
Öz
ÖZ
Arı ürünlerinin insan sağlığı üzerindeki olumlu etkileri, antioksidan bileşimlerinden kaynaklan-maktadır. Ancak insan eritrositleri üzerinde t-butilhidroksiperoksit (t-BHP) kaynaklı oksidatif hasara karşı olası koruyucu etkinlikleri araştırılmamıştır. Bu çalışmadaki amacımız propolis, polen ve arı sütünün, izole edilen eritrositlerde t-BHP indüklü oksidatif hasara karşı koruyucu etkinliğe sahip olup olmadığını araştırmaktır. Türkiye’nin çeşitli bölgelerinden toplanan propolis ve polen örnekleri çeşitli solventler (su ve etanol) ile karıştırılarak ekstrakte edildi. Ticari olarak satın alınan arı sütü de su ile ekstrakte edildi. 15 gönüllüden toplanılan eritrositler santrifüj edildi ve izotonik tuzla yıkanılarak paketlendi. Tüm RBC paketleri bir araya toplandı ve kontrol, sulu propolis ekstraktı, etanollü propolis ekstraktı, sulu polen ekstraktı, sulu arı sütü ekstraktı, pozitif kontrol (kuersetin) ve t-BHP ile olmak üzere yedi gruba ayrıldı. Eritrositler ilk olarak arı ürünlerinin ekstraktları ile muamele edilmiştir ve daha sonra t-BHP eklenmiştir. Arı ürünlerinin koruyucu etkinlikleri, malondialdehit (MDA), toplam oksidan kapasite (TOK), toplam antioksidan kapasite (TAK), süperoksit dismutaz (SOD) ve katalaz (KAT) aktiviteleri ile araştırıldı. İstatistiksel olarak, ANOVA ve post-hoc Tukey testleri uygulandı. Çalışma sonucunda tüm arı ürünlerinin MDA seviyelerini kontrol grubuna yakın seviyelerde kalmasına katkı sağladığı bulunmuştur. (p<0.05). Yine tüm arı ürünlerinin t-BHP grubuna göre TOK düzeylerini düşerken TAK düzeyleri ise yükselmiştir (p<0.05). Arı ürünlerinin SOD ve KAT seviyeleri üzerinde önemli bir etkisi gözlenmedi (p>0.05).
Destekleyen Kurum
KARADENİZ TEKNİK ÜNİVERSİTESİ BİLİMSEL ARAŞTIRMA PROJELERİ KOORDİNASYON BİRİMİ
Proje Numarası
TYL-2018-6804
Kaynakça
- 1. Teixeira, E.W, Message, D, Negri, G, Salatino, A. and Stringheta, P.C. (2010). ‘‘Seasonal variation, chemical composition and antioxidant activity of Brazilian propolis samples’’. Evid Based Complement Alternat Med, 7 (3), 307-15. doi: 10.1093/ecam/nem177.
- 2. Bankova, V, Boudourova-Krasteva, G, Sforcin, J.M, Frete, X, Kujumgiev, A, Maimoni-Rodella, R. and Popov, S. (1999). ‘‘Phytochemical evidence for the plant origin of Brazilian propolis from São Paulo state’’. Z Naturforsch C J Biosci, 54 (5-6), 401-5. doi: 10.1515/znc-1999-5-616.
- 3. Banskota, A.H, Tezuka, Y. and Kadota, S. (2001). ‘‘Recent progress in pharmacological research of propolis’’. Phytother Res Nov, 15 (7), 561-71. doi: 10.1002/ptr.1029.
- 4. Sforcin, J.M. (2007). ‘‘Propolis and the immune system: a review’’. J Ethnopharmacol, 15, 113 (1), 1-14. doi: 10.1016/j.jep.2007.05.012.
- 5. Sforcin, J.M. and Bankova, V. (2011). ‘‘Propolis: is there a potential for the development of new drugs’’. J Ethnopharmacol, 27, 133 (2), 253-60. doi: 10.1016/j.jep.2010.10.032.
- 6. Sforcin, J.M. (2016). ‘‘Biological Properties and Therapeutic Applications of Propolis’’. Phytother Res Jun, 30 (6), 894-905. doi: 10.1002/ptr.5605.
- 7. Ishikawa, Y, Tokura, T, Nakano, N, Hara, M, Niyonsaba, F. and Ushio, H. (2008). ‘‘Inhibitory effect of honeybee-collected pollen on mast cell degranulation in vivo and in vitro’’. J Med Food, 11 (1), 14-20. doi: 10.1089/jmf.2006.163.
- 8. Rzepecka-Stojko, A, Stojko, J, Kurek-Górecka, A, Górecki, M, Kabała-Dzik, A, Kubina, R, Moździerz, A. and Buszman, E. (2015). ‘‘Polyphenols from Bee Pollen: Structure, Absorption, Metabolism and Biological Activity’’. Molecules Dec 4, 20 (12), 21732-49. doi: 10.3390/molecules201219800.
- 9. Geethangili, M. and Ding, S.T. (2018). ‘‘A Review of the Phytochemistry and Pharmacology of Phyllanthus urinaria L. Frontiers in pharmacology’’. 9, 1109. doi: 10.3389/fphar.2018.01109.
- 10. Han, X, Shen, T. and Lou, H. (2007). ‘‘Dietary Polyphenols and Their Biological Significance’’. International Journal of Molecular Sciences, 8 (9), 950–988.
- 11. Viuda-Martos, M, Ruiz-Navajas, Y, Fernández-López, J. and Pérez-Alvarez, J.A. (2008). ‘‘Functional properties of honey, propolis, and royal jelly’’. J Food Sci Nov, 73 (9), 117-24. doi: 10.1111/j.1750-3841.2008.00966.x.
- 12. Klaunig, J.E, Kamendulis, L.M. and Hocevar, B.A. (2010). ‘‘Oxidative stress and oxidative damage in carcinogenesis’’. Toxicol Pathol, 38 (1), 96-109. doi: 10.1177/0192623309356453.
- 13. Valko, M, Rhodes, C.J, Moncol, J, Izakovic, M. and Mazur, M. (2006). ‘‘Free radicals, metals and antioxidants in oxidative stress-induced cancer’’. Chem Biol Interact, 10, 160 (1), 1-40. doi: 10.1016/j.cbi.2005.12.009.
- 14. Valko, M, Leibfritz, D, Moncol, J, Cronin, M.T, Mazur, M. and Telser, J. (2007). ‘‘Free radicals and antioxidants in normal physiological functions and human disease’’. Int J Biochem Cell Biol, 39 (1), 44-84. doi: 10.1016/j.biocel.2006.07.001.
- 15. Azzi, A. (2007). ‘‘Oxidative stress: A dead end or a laboratory hypothesis’’. Biochem Biophys Res Commun, 19, 362 (2), 230-2. doi: 10.1016/j.bbrc.2007.07.124.
- 16. Halliwell, B. and Aruoma, O.I. (1991). ‘‘DNA damage by oxygen-derived species. Its mechanism and measurement in mammalian systems’’. FEBS Lett Apr, 9, 281 (1-2), 9-19. doi: 10.1016/0014-5793(91), 80347-6.
- 17. Lobo, V, Patil, A, Phatak, A. and Chandra, N. (2010). ‘‘Free radicals, antioxidants and functional foods: Impact on human health’’. Pharmacognosy reviews, 4 (8), 118–126. doi: 10.4103/0973-7847.70902.
- 18. Reeg, S. and Grune, T. (2015). ‘‘Protein Oxidation in Aging: Does It Play a Role in Aging Progression’’. Antioxid Redox Signal, 20, 23 (3), 239-55. doi: 10.1089/ars.2014.6062.
- 19. Stadtman, E.R. and Levine, R.L. (2003). ‘‘Free radical-mediated oxidation of free amino acids and amino acid residues in proteins’’. Amino Acids Dec, 25 (3-4), 207-18. doi: 10.1007/s00726-003-0011-2.
- 20. Catalá, A. (2009). ‘‘Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions’’. Chem Phys Lipids, 157 (1), 1-11. doi: 10.1016/j.chemphyslip.2008.09.004.
- 21. Lima, C.F, Fernandes-Ferreira, M. and Pereira-Wilson, C. (2006). ‘‘Phenolic compounds protect HepG2 cells from oxidative damage: relevance of glutathione levels’’. Life Sci, 19, 79 (21), 2056-68. doi: 10.1016/j.lfs.2006.06.042.
- 22. Maurya, P.K, Kumar, P. and Chandra, P. (2015). ‘‘Biomarkers of oxidative stress in erythrocytes as a function of human age’’. World J Methodol, 26, 5 (4), 216-22. doi: 10.5662/wjm.v5.i4.216.
- 23. Kocot, J, Kiełczykowska, M, Luchowska-Kocot, D, Kurzepa, J. and Musik, I. (2018). ‘‘Antioxidant Potential of Propolis, Bee Pollen, and Royal Jelly: Possible Medical Application’’. Oxid Med Cell Longev, 2, 2018-7074209. doi: 10.1155/2018/7074209.
- 24. Stocks, J. and Dormandy, T.L. (1971). ‘‘The autoxidation of human red cell lipids induced by hydrogen peroxide’’. Br J Haematol, 20, 95-111. doi: 10.1111/j.1365-2141.1971.tb00790.x.
- 25. Erel, O. (2005). ‘‘A new automated colorimetric method for measuring total oxidant status’’. Clin Biochem Dec, 38 (12), 1103-11. doi: 10.1016/j.clinbiochem.2005.08.008.
- 26. Erel, O. (2004). ‘‘A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation’’. Clin Biochem Apr, 37 (4), 277-85. doi: 10.1016/j.clinbiochem.2003.11.015.
- 27. Sun, Y, Oberley, L.W. and Li, Y. (1988). ‘‘A simple method for clinical assay of superoxide dismutase’’. Clin Chem, 34 (3), 497-500. doi: 10.1093/clinchem/34.3.497.
- 28. Goth, L. (1991). ‘‘A simple method for determination of serum catalase activity and revision of reference range’’. Clin Chim Acta, 15, 196 (2-3), 143-51. doi: 10.1016/0009-8981(91)90067-m.
- 29. Kucuk, M, Karaoglu, S, Ulusoy, E, Baltaci, C. ve Candan, F. (2007). ‘‘Biological activities and chemical composition of three honeys of different types from Anatolia’’. Food Chem, 100, 526–534. doi: 10.1016/j.foodchem.2005.10.010.
- 30. Tahir, H.E, Xiaobo, Z, Zhihua, L, Jiyong, S, Zhai, X, Wang, S. and Mariod, A.A. (2017). ‘‘Rapid prediction of phenolic compounds and antioxidant activity of Sudanese honey using’’. Food Chem, 1, 226, 202-211. doi: 10.1016/j.foodchem.2017.01.024.
- 31. Bartkiene, E, Lele, V, Sakiene, V, Zavistanaviciute, P, Zokaityte, E. and Dauksiene, A. (2020). ‘‘Variations of the antimicrobial, antioxidant, sensory attributes and biogenic amines content in Lithuania-derived bee products’’. LWT Food Sci Technol, 118, 108793. doi: 10.1016/j.lwt.2019.108793.
- 32. Viuda-Martos, M, Ruiz-Navajas, Y, Fernández-López, J. and Pérez-Alvarez, J.A. (2008). ‘‘Functional properties of honey, propolis, and royal jelly’’. J Food Sci, 73 (9), 117-24. doi: 10.1111/j.1750-3841.2008.00966.x.
- 33. Moreira, L.L, Dias, T, Dias, L.G, Rogão, M, Da Silva, J.P. and Estevinho, L.M. (2011). ‘‘Propolis influence on erythrocyte membrane disorder (hereditary spherocytosis): a first approach’’. Food Chem Toxicol, 49 (2), 520-6. doi: 10.1016/j.fct.2010.11.042.
- 34. Mujica, V, Orrego, R, Pérez, J, Romero, P, Ovalle, P. and Zúñiga-Hernández, J. (2017). ‘‘The Role of Propolis in Oxidative Stress and Lipid Metabolism: A Randomized Controlled Trial’’. Evid Based Complement Alternat Med, 2017, 4272940. doi: 10.1155/2017/4272940.
- 35. Jasprica, I, Mornar, A, Debeljak, Z, Smolcić-Bubalo, A, Medić-Sarić, M. and Mayer, L. (2007). ‘‘In vivo study of propolis supplementation effects on antioxidative status and red blood cells’’. J Ethnopharmacol, 4, 110 (3), 548-54. doi: 10.1016/j.jep.2006.10.023.
- 36. Bazmandegan, G, Boroushaki, M.T, Shamsizadeh, A, Ayoobi, F, Hakimizadeh, E. and Allahtavakoli, M. (2017). ‘‘Brown propolis attenuates cerebral ischemia-induced oxidative damage via affecting antioxidant enzyme system in mice’’. Biomed Pharmacother, 85, 503-510. doi: 10.1016/j.biopha.2016.11.057.
- 37. Ishikawa, Y, Tokura, T, Ushio, H, Niyonsaba, F, Yamamoto, Y, Tadokoro, T, Ogawa, H. and Okumura, K. (2009). ‘‘Lipid-soluble components of honeybee-collected pollen exert antiallergic effect by inhibiting IgE-mediated mast cell activation in vivo’’. Phytother Res, 23 (11), 1581-6. doi: 10.1002/ptr.2824.
- 38. Slamenova, D, Kozics, K, Hunakova, L, Melusova, M, Navarova, J. and Horvathova, E. (2013). ‘‘Comparison of biological processes induced in HepG2 cells by tert-butyl hydroperoxide (t-BHP) and hydroperoxide (H2O2): The influence of carvacrol’’. Mutat Res, 18, 757 (1), 15-22. doi: 10.1016/j.mrgentox.2013.03.014.
- 39. Bonamigo, T, Campos, J.F, Alfredo, T.M, Balestieri, J.B, Cardoso, C.A, Paredes-Gamero, E.J, de Picoli Souza, K. and Dos Santos, E.L. (2017). ‘‘Antioxidant, cytotoxic, and toxic activities of propolis from two native bees in Brazil: scaptotrigona depilis and Melipona quadrifasciata anthidioides’’. Oxid Med Cell Longev, 1038153, 12. doi: 10.1155/2017/1038153.
Protective Effect of Bee Products Against Oxidative Damage in Erythrocytes
Yıl 2023,
Cilt: 12 Sayı: 1, 167 - 174, 25.03.2023
Orhan Değer
,
Ertuğrul Yiğit
,
Katip Korkmaz
,
Pınar Aygün
,
Ali Asghari
,
Kübra Akbulut Çakıroğlu
,
Selim Demir
Öz
The positive effects of bee products on human health are due to their antioxidant composition. However, their possible protective efficacy against t-butylhydroxyperoxide (t-BHP)-induced oxidative damage on human erythrocytes has not been investigated. Our aim in this study is to investigate whether propolis, pollen and royal jelly have protective efficacy against t-BHP-induced oxidative damage in isolated erythrocytes. Propolis and pollen samples collected from various regions of Turkey were extracted by mixing with various solvents (water and ethanol). Commercially purchased royal jelly was also extracted with water. The erythrocytes collected from 15 volunteers were centrifuged and packaged by washing with isotonic saline. All RBC packets were pooled together. The final erythrocyte packet was divided into seven groups as control, water extract of propolis, ethanolic extract of propolis, water extract of pollen, water extract of royal jelly, positive control (quercetin) and t-BHP groups. Erythrocytes were first treated with extracts of bee products and then t-BHP was added. Protective activities of bee products were investigated by malondialdehyde (MDA), total oxidant capacity (TOS), total antioxidant capacity (TAS), superoxide dismutase (SOD) and catalase (CAT) activities. Statistically, one way ANOVA and post-hoc Tukey tests were applied. As a result of the study, it was found that all bee products contributed to keeping MDA levels close to the control group. (p<0.05). Again, while TOS levels of all bee products decreased compared to t-BHP, TAS levels increased (p<0.05). No significant effect of bee products on SOD and CAT enzyme activities was observed. (p>0.05).
Proje Numarası
TYL-2018-6804
Kaynakça
- 1. Teixeira, E.W, Message, D, Negri, G, Salatino, A. and Stringheta, P.C. (2010). ‘‘Seasonal variation, chemical composition and antioxidant activity of Brazilian propolis samples’’. Evid Based Complement Alternat Med, 7 (3), 307-15. doi: 10.1093/ecam/nem177.
- 2. Bankova, V, Boudourova-Krasteva, G, Sforcin, J.M, Frete, X, Kujumgiev, A, Maimoni-Rodella, R. and Popov, S. (1999). ‘‘Phytochemical evidence for the plant origin of Brazilian propolis from São Paulo state’’. Z Naturforsch C J Biosci, 54 (5-6), 401-5. doi: 10.1515/znc-1999-5-616.
- 3. Banskota, A.H, Tezuka, Y. and Kadota, S. (2001). ‘‘Recent progress in pharmacological research of propolis’’. Phytother Res Nov, 15 (7), 561-71. doi: 10.1002/ptr.1029.
- 4. Sforcin, J.M. (2007). ‘‘Propolis and the immune system: a review’’. J Ethnopharmacol, 15, 113 (1), 1-14. doi: 10.1016/j.jep.2007.05.012.
- 5. Sforcin, J.M. and Bankova, V. (2011). ‘‘Propolis: is there a potential for the development of new drugs’’. J Ethnopharmacol, 27, 133 (2), 253-60. doi: 10.1016/j.jep.2010.10.032.
- 6. Sforcin, J.M. (2016). ‘‘Biological Properties and Therapeutic Applications of Propolis’’. Phytother Res Jun, 30 (6), 894-905. doi: 10.1002/ptr.5605.
- 7. Ishikawa, Y, Tokura, T, Nakano, N, Hara, M, Niyonsaba, F. and Ushio, H. (2008). ‘‘Inhibitory effect of honeybee-collected pollen on mast cell degranulation in vivo and in vitro’’. J Med Food, 11 (1), 14-20. doi: 10.1089/jmf.2006.163.
- 8. Rzepecka-Stojko, A, Stojko, J, Kurek-Górecka, A, Górecki, M, Kabała-Dzik, A, Kubina, R, Moździerz, A. and Buszman, E. (2015). ‘‘Polyphenols from Bee Pollen: Structure, Absorption, Metabolism and Biological Activity’’. Molecules Dec 4, 20 (12), 21732-49. doi: 10.3390/molecules201219800.
- 9. Geethangili, M. and Ding, S.T. (2018). ‘‘A Review of the Phytochemistry and Pharmacology of Phyllanthus urinaria L. Frontiers in pharmacology’’. 9, 1109. doi: 10.3389/fphar.2018.01109.
- 10. Han, X, Shen, T. and Lou, H. (2007). ‘‘Dietary Polyphenols and Their Biological Significance’’. International Journal of Molecular Sciences, 8 (9), 950–988.
- 11. Viuda-Martos, M, Ruiz-Navajas, Y, Fernández-López, J. and Pérez-Alvarez, J.A. (2008). ‘‘Functional properties of honey, propolis, and royal jelly’’. J Food Sci Nov, 73 (9), 117-24. doi: 10.1111/j.1750-3841.2008.00966.x.
- 12. Klaunig, J.E, Kamendulis, L.M. and Hocevar, B.A. (2010). ‘‘Oxidative stress and oxidative damage in carcinogenesis’’. Toxicol Pathol, 38 (1), 96-109. doi: 10.1177/0192623309356453.
- 13. Valko, M, Rhodes, C.J, Moncol, J, Izakovic, M. and Mazur, M. (2006). ‘‘Free radicals, metals and antioxidants in oxidative stress-induced cancer’’. Chem Biol Interact, 10, 160 (1), 1-40. doi: 10.1016/j.cbi.2005.12.009.
- 14. Valko, M, Leibfritz, D, Moncol, J, Cronin, M.T, Mazur, M. and Telser, J. (2007). ‘‘Free radicals and antioxidants in normal physiological functions and human disease’’. Int J Biochem Cell Biol, 39 (1), 44-84. doi: 10.1016/j.biocel.2006.07.001.
- 15. Azzi, A. (2007). ‘‘Oxidative stress: A dead end or a laboratory hypothesis’’. Biochem Biophys Res Commun, 19, 362 (2), 230-2. doi: 10.1016/j.bbrc.2007.07.124.
- 16. Halliwell, B. and Aruoma, O.I. (1991). ‘‘DNA damage by oxygen-derived species. Its mechanism and measurement in mammalian systems’’. FEBS Lett Apr, 9, 281 (1-2), 9-19. doi: 10.1016/0014-5793(91), 80347-6.
- 17. Lobo, V, Patil, A, Phatak, A. and Chandra, N. (2010). ‘‘Free radicals, antioxidants and functional foods: Impact on human health’’. Pharmacognosy reviews, 4 (8), 118–126. doi: 10.4103/0973-7847.70902.
- 18. Reeg, S. and Grune, T. (2015). ‘‘Protein Oxidation in Aging: Does It Play a Role in Aging Progression’’. Antioxid Redox Signal, 20, 23 (3), 239-55. doi: 10.1089/ars.2014.6062.
- 19. Stadtman, E.R. and Levine, R.L. (2003). ‘‘Free radical-mediated oxidation of free amino acids and amino acid residues in proteins’’. Amino Acids Dec, 25 (3-4), 207-18. doi: 10.1007/s00726-003-0011-2.
- 20. Catalá, A. (2009). ‘‘Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions’’. Chem Phys Lipids, 157 (1), 1-11. doi: 10.1016/j.chemphyslip.2008.09.004.
- 21. Lima, C.F, Fernandes-Ferreira, M. and Pereira-Wilson, C. (2006). ‘‘Phenolic compounds protect HepG2 cells from oxidative damage: relevance of glutathione levels’’. Life Sci, 19, 79 (21), 2056-68. doi: 10.1016/j.lfs.2006.06.042.
- 22. Maurya, P.K, Kumar, P. and Chandra, P. (2015). ‘‘Biomarkers of oxidative stress in erythrocytes as a function of human age’’. World J Methodol, 26, 5 (4), 216-22. doi: 10.5662/wjm.v5.i4.216.
- 23. Kocot, J, Kiełczykowska, M, Luchowska-Kocot, D, Kurzepa, J. and Musik, I. (2018). ‘‘Antioxidant Potential of Propolis, Bee Pollen, and Royal Jelly: Possible Medical Application’’. Oxid Med Cell Longev, 2, 2018-7074209. doi: 10.1155/2018/7074209.
- 24. Stocks, J. and Dormandy, T.L. (1971). ‘‘The autoxidation of human red cell lipids induced by hydrogen peroxide’’. Br J Haematol, 20, 95-111. doi: 10.1111/j.1365-2141.1971.tb00790.x.
- 25. Erel, O. (2005). ‘‘A new automated colorimetric method for measuring total oxidant status’’. Clin Biochem Dec, 38 (12), 1103-11. doi: 10.1016/j.clinbiochem.2005.08.008.
- 26. Erel, O. (2004). ‘‘A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation’’. Clin Biochem Apr, 37 (4), 277-85. doi: 10.1016/j.clinbiochem.2003.11.015.
- 27. Sun, Y, Oberley, L.W. and Li, Y. (1988). ‘‘A simple method for clinical assay of superoxide dismutase’’. Clin Chem, 34 (3), 497-500. doi: 10.1093/clinchem/34.3.497.
- 28. Goth, L. (1991). ‘‘A simple method for determination of serum catalase activity and revision of reference range’’. Clin Chim Acta, 15, 196 (2-3), 143-51. doi: 10.1016/0009-8981(91)90067-m.
- 29. Kucuk, M, Karaoglu, S, Ulusoy, E, Baltaci, C. ve Candan, F. (2007). ‘‘Biological activities and chemical composition of three honeys of different types from Anatolia’’. Food Chem, 100, 526–534. doi: 10.1016/j.foodchem.2005.10.010.
- 30. Tahir, H.E, Xiaobo, Z, Zhihua, L, Jiyong, S, Zhai, X, Wang, S. and Mariod, A.A. (2017). ‘‘Rapid prediction of phenolic compounds and antioxidant activity of Sudanese honey using’’. Food Chem, 1, 226, 202-211. doi: 10.1016/j.foodchem.2017.01.024.
- 31. Bartkiene, E, Lele, V, Sakiene, V, Zavistanaviciute, P, Zokaityte, E. and Dauksiene, A. (2020). ‘‘Variations of the antimicrobial, antioxidant, sensory attributes and biogenic amines content in Lithuania-derived bee products’’. LWT Food Sci Technol, 118, 108793. doi: 10.1016/j.lwt.2019.108793.
- 32. Viuda-Martos, M, Ruiz-Navajas, Y, Fernández-López, J. and Pérez-Alvarez, J.A. (2008). ‘‘Functional properties of honey, propolis, and royal jelly’’. J Food Sci, 73 (9), 117-24. doi: 10.1111/j.1750-3841.2008.00966.x.
- 33. Moreira, L.L, Dias, T, Dias, L.G, Rogão, M, Da Silva, J.P. and Estevinho, L.M. (2011). ‘‘Propolis influence on erythrocyte membrane disorder (hereditary spherocytosis): a first approach’’. Food Chem Toxicol, 49 (2), 520-6. doi: 10.1016/j.fct.2010.11.042.
- 34. Mujica, V, Orrego, R, Pérez, J, Romero, P, Ovalle, P. and Zúñiga-Hernández, J. (2017). ‘‘The Role of Propolis in Oxidative Stress and Lipid Metabolism: A Randomized Controlled Trial’’. Evid Based Complement Alternat Med, 2017, 4272940. doi: 10.1155/2017/4272940.
- 35. Jasprica, I, Mornar, A, Debeljak, Z, Smolcić-Bubalo, A, Medić-Sarić, M. and Mayer, L. (2007). ‘‘In vivo study of propolis supplementation effects on antioxidative status and red blood cells’’. J Ethnopharmacol, 4, 110 (3), 548-54. doi: 10.1016/j.jep.2006.10.023.
- 36. Bazmandegan, G, Boroushaki, M.T, Shamsizadeh, A, Ayoobi, F, Hakimizadeh, E. and Allahtavakoli, M. (2017). ‘‘Brown propolis attenuates cerebral ischemia-induced oxidative damage via affecting antioxidant enzyme system in mice’’. Biomed Pharmacother, 85, 503-510. doi: 10.1016/j.biopha.2016.11.057.
- 37. Ishikawa, Y, Tokura, T, Ushio, H, Niyonsaba, F, Yamamoto, Y, Tadokoro, T, Ogawa, H. and Okumura, K. (2009). ‘‘Lipid-soluble components of honeybee-collected pollen exert antiallergic effect by inhibiting IgE-mediated mast cell activation in vivo’’. Phytother Res, 23 (11), 1581-6. doi: 10.1002/ptr.2824.
- 38. Slamenova, D, Kozics, K, Hunakova, L, Melusova, M, Navarova, J. and Horvathova, E. (2013). ‘‘Comparison of biological processes induced in HepG2 cells by tert-butyl hydroperoxide (t-BHP) and hydroperoxide (H2O2): The influence of carvacrol’’. Mutat Res, 18, 757 (1), 15-22. doi: 10.1016/j.mrgentox.2013.03.014.
- 39. Bonamigo, T, Campos, J.F, Alfredo, T.M, Balestieri, J.B, Cardoso, C.A, Paredes-Gamero, E.J, de Picoli Souza, K. and Dos Santos, E.L. (2017). ‘‘Antioxidant, cytotoxic, and toxic activities of propolis from two native bees in Brazil: scaptotrigona depilis and Melipona quadrifasciata anthidioides’’. Oxid Med Cell Longev, 1038153, 12. doi: 10.1155/2017/1038153.