Comprehensive Study on BeeBread: Palynological Analysis, Chemical Composition, Antioxidant and Cytotoxic Activities
Year 2022,
Volume: 9 Issue: 2, 166 - 177, 15.06.2022
Gökhan Dervişoğlu
,
Duygu Nur Çobanoğlu
,
Sedat Yelkovan
,
Davut Karahan
,
Yusuf Çakır
,
Serhat Koçyiğit
Abstract
Bee bread is a bee product obtained as a result of fermentation of pollen stored by honey bees in the cells of the honeycomb. Palynological analysis, chemical composition, antioxidant activity of bee bread and its cytotoxic effect against human lung carcinoma (A549), human prostate cancer (DU 145) and human neuroblastoma (SH-SY5Y) cell lines were investigated in this study. 25 plant taxa were identified with palynological analysis. Fatty acids, cyclic, aromatic, phenolic, terpenoid, diterpen and metallic complex structures were seen in GC-MS results. FTIR consequence were compatible with GC-MS results and the structure types of FTIR results were seen in the dominant compounds of GC-MS results. Radical scavenging activity (RSA) of bee bread showed inhibition variability between 20.15 ± 0.68% and 93.18 ± 0.44% depending on the concentration. In addition, the EC50 value was measured as 80.08 ± 0.10 mg/mL. Bee bread exhibited moderately cytotoxic effect at all concentrations (15.625 - 2000 µg/mL) against A549, DU 145, and SH-SY5Y cell lines. Bee bread can be used in medical fields because of it’s antioxidant and anticancer properties.
References
- Akbari, S., Abdurahman, N.H., Yunus, R.M., Alara, O.R., & Abayomi, O.O. (2019). Extraction, characterization and antioxidant activity of fenugreek (Trigonella-foenum graecum) seed oil. Materials Science for Energy Technologies, 2(2), 349-355.
- Bakour, M., Fernandes, Â., Barros, L., Sokovic, M., & Ferreira, I.C. (2019). Bee bread as a functional product: Chemical composition and bioactive properties. LWT, 109, 276-282.
- Barbarić, M., Mišković, K., Bojić, M., Lončar, M.B., Smolčić-Bubalo, A., Debeljak, Ž., & Medić-Šarić, M. (2011). Chemical composition of the ethanolic propolis extracts and its effect on HeLa cells. Journal of Ethnopharmacology, 135(3), 772-778.
- Behçet, L., & Yapar, Y. (2019). Important plants at the Matan Mountain (Bingöl/Turkey) flora with regard to beekeeping. Biological Diversity and Conservation, 12(1), 149-159.
- Bobiş, O., Mărghitaş, L.A., Dezmirean, D., Morar, O., Bonta, V., & Chirilă, F. (2010). Quality parameters and nutritional value of different commercial bee products. Bulletin UASVM Animal Science and Biotechnologies, 67, 1-2.
- Borawska, M.H., Markiewicz-Żukowska, R., Naliwajko, S.K., Moskwa, J., Bartosiuk, E., Socha, K., . . . Mariak, Z. (2014). The interaction of bee products with temozolomide in human diffuse astrocytoma, glioblastoma multiforme and astroglia cell lines. Nutrition and cancer, 66(7), 1247-1256.
- Borges, K.S., Brassesco, M.S., Scrideli, C.A., Soares, A.E.E., & Tone, L.G. (2011). Antiproliferative effects of Tubi-bee propolis in glioblastoma cell lines. Genetics and Molecular Biology, 34, 310-314.
- Chandrasekaran, M., Kannathasan, K., & Venkatesalu, V. (2008). Antimicrobial activity of fatty acid methyl esters of some members of Chenopodiaceae. Zeitschrift für Naturforschung C, 63(5-6), 331-336.
- Çakır, Y., Çobanoğlu, D.N., Dervişoğlu, G., Koçyiğit, S., Karahan, D., & Yelkovan, S. (2020). Determination Antimicrobial Activity, Palynological Characteristics and Chemical Composition of Some Honey Samples from Turkey. Mellifera, 20(1), 41-60.
- da Silva Frozza, C.O., Garcia, C.S.C., Gambato, G., de Souza, M.D.O., Salvador, M., Moura, S., . . . Borsuk, S. (2013). Chemical characterization, antioxidant and cytotoxic activities of Brazilian red propolis. Food and Chemical Toxicology, 52, 137-142.
- Ergun, M., Süslüoğlu, Z., & Bengü, A.Ş. (2017). Studying Structural Differentiation of Plant Parts of Sideritis pisidica Boiss. & Heldr. Using FTIR Spectroscopy. Türk Tarım ve Doğa Bilimleri Dergisi, 4(4), 461-467.
- Etehadpour, M., & Tavassolian, I. (2019). Ecological factors regulate essential oil yield, percent and compositions of endemic yarrow (Achillea eriophora DC.) in Southeast Iran. International Journal of Horticultural Science and Technology, 6(2), 201-215.
- Ferlay, J., Soerjomataram, I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., . . . Bray, F. (2015). Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. International journal of cancer, 136(5), E359-E386.
- Ghosh, K., & Indra, N. (2014). Phytochemistry, in vitro free radical scavenging, chelating and toxicity of Centela asiatica L.(Apiaceae) ethanolic leaf extract. International Journal of Pharmaceutical Sciences Review and Research, 29, 328-334.
- Gilliam, M. (1979). Microbiology of pollen and bee bread: the yeasts. Apidologie, 10(1), 43-53.
- Giroud, B., Vauchez, A., Vulliet, E., Wiest, L., & Buleté, A. (2013). Trace level determination of pyrethroid and neonicotinoid insecticides in beebread using acetonitrile-based extraction followed by analysis with ultra-high-performance liquid chromatography–tandem mass spectrometry. Journal of Chromatography A, 1316, 53-61.
- Greenland, G.J., & Bowden, B.F. (1994). Cembranoid diterpenes related to sarcophytol A from the soft coral Sarcophyton trocheliophorum (Alcyonacea). Australian Journal of Chemistry, 47(11), 2013-2021.
- Hatano, T., Kagawa, H., Yasuhara, T., & Okuda, T. (1988). Two new flavonoids and other constituents in licorice root: their relative astringency and radical scavenging effects. Chemical and pharmaceutical bulletin, 36(6), 2090-2097.
- Heck, J.E., Ritz, B., Hung, R.J., Hashibe, M., & Boffetta, P. (2009). The epidemiology of neuroblastoma: a review. Paediatric and perinatal epidemiology, 23(2), 125-143.
- Jemal, A., Bray, F., Center, M.M., Ferlay, J., Ward, E., & Forman, D. (2011). Global cancer statistics. CA: a cancer journal for clinicians, 61(2), 69-90.
- Kaplan, M., Karaoğlu, Ö., & Silici, S. (2019). An Evaluation on Bee Bread: Chemical and Palynological Analysis. Mellifera, 19(1), 21-29.
- Kaya, B., Darendelioğlu, E., Dervişoğlu, G., & Tartik, M. (2018). Determination of comparative biological activities of silver nanoparticles formed by biological synthesis using Achillea Vermicularis. Pak. J. Bot, 50(4), 1423-1432.
- Khan, F., Abdullah Asuhaimi, F., Jalal, T.K., Roheem, F.O., Natto, H.A., Johan, M.F., . . . Abdul Wahab, R. (2019). Hystrix Brachyura Bezoar Characterization, Antioxidant Activity Screening, and Anticancer Activity on Melanoma Cells (A375): A Preliminary Study. Antioxidants, 8(2), 39.
- Kostova, I. (2006). Ruthenium complexes as anticancer agents. Current medicinal chemistry, 13(9), 1085-1107.
- Kuptsov, A., & Zhizhin, G.N. (1998). Handbook of Fourier transform Raman and infrared spectra of polymers. Elsevier.
- Li, X., Wang, Z.G., Chen, H.H., & Liu, S.G. (2014). The antioxidant methyl 3-(3,5-di-tert-butyl-4-hydroxyphenyl)propionate. Acta Crystallogr C Struct Chem, 70(Pt 11), 1050-1053. https://doi.org/10.1107/s2053229614021445
- Liu, X.D., Zhang, F.B., Zhou, B., Shan, H., & Chen, P.Y. (2015). Effect of sonication on different quality parameters of Pinus massoniana pollen. Ultrasonics sonochemistry, 22, 174-181.
- Luz, C.F.P.D., & Barth, O.M. (2012). Pollen analysis of honey and beebread derived from Brazilian mangroves. Brazilian Journal of Botany, 35(1), 79-85.
- Magalhães, L.M., Segundo, M.A., Reis, S., & Lima, J.L. (2008). Methodological aspects about in vitro evaluation of antioxidant properties. Analytica chimica acta, 613(1), 1-19.
- Mărgăoan, R., Stranț, M., Varadi, A., Topal, E., Yücel, B., Cornea-Cipcigan, M., . . . Vodnar, D.C. (2019). Bee collected pollen and bee bread: Bioactive constituents and health benefits. Antioxidants, 8(12), 568.
- Markiewicz-Żukowska, R., Naliwajko, S.K., Bartosiuk, E., Moskwa, J., Isidorov, V., Soroczyńska, J., & Borawska, M.H. (2013). Chemical composition and antioxidant activity of beebread, and its influence on the glioblastoma cell line (U87MG). Journal of Apicultural Science, 57(2), 147-157. https://doi.org/doi:10.2478/jas-2013-0025
- Mayda, N., Özkök, A., Bayram, N.E., Gerçek, Y.C., & Sorkun, K. (2020). Bee bread and bee pollen of different plant sources: Determination of phenolic content, antioxidant activity, fatty acid and element profiles. Journal of Food Measurement and Characterization, 14(4), 1795-1809.
- Pinto, M.E., Araujo, S.G., Morais, M.I., Sá, N.P., Lima, C.M., Rosa, C.A., . . . Lima, L.A. (2017). Antifungal and antioxidant activity of fatty acid methyl esters from vegetable oils. Anais da Academia Brasileira de Ciências, 89, 1671-1681.
- Reedijk, B.J. (2008). Metal-ligand exchange kinetics in platinum and ruthenium complexes. Platinum Metals Review, 52(1), 2-11.
- Sobral, F., Calhelha, R.C., Barros, L., Dueñas, M., Tomás, A., Santos-Buelga, C., . . . Ferreira, I.C. (2017). Flavonoid composition and antitumor activity of bee bread collected in northeast Portugal. Molecules, 22(2), 248.
- Soumya, V., Muzib, Y.I., Venkatesh, P., & Hariprasath, K. (2014). GC-MS analysis of Cocus nucifera flower extract and its effects on heterogeneous symptoms of polycystic ovarian disease in female Wistar rats. Chinese journal of natural medicines, 12(9), 677-684.
- Sreeramulu, D., Reddy, C., Chauhan, A., Balakrishna, N., & Raghunath, M. (2013). Natural antioxidant activity of commonly consumed plant foods in India: effect of domestic processing. Oxidative Medicine and Cellular Longevity, 2013.
- Syamdidi, H.E.I., & Irianto, G. (2016). Agar-abundant Marine Carbohydrate from Seaweeds in Indonesia: Production, Bioactivity, and Utilization. In Marine Glycobiology (pp. 275-282). CRC Press.
- Tuzcu, Z., Koclar, G., Agca, C.A., Aykutoglu, G., Dervisoglu, G., Tartik, M., . . . Sahin, K. (2017). Antioxidant, antimicrobial and anticancer effects of different extracts from wild edible plant Eremurus spectabilis leaves and roots. International journal of clinical and experimental medicine, 10(3), 4787-4797.
- Wróblewska, A., Warakomska, Z., & Koter, M. (2006). Pollen analysis of bee products from the north-eastern Poland. Journal of Apicultural Science, 50(1), 71-83.
- Yang, X., Guo, D., Zhang, J., & Wu, M. (2007). Characterization and anti-tumor activity of pollen polysaccharide. International immunopharmacology, 7(3), 401-408.
Comprehensive Study on BeeBread: Palynological Analysis, Chemical Composition, Antioxidant and Cytotoxic Activities
Year 2022,
Volume: 9 Issue: 2, 166 - 177, 15.06.2022
Gökhan Dervişoğlu
,
Duygu Nur Çobanoğlu
,
Sedat Yelkovan
,
Davut Karahan
,
Yusuf Çakır
,
Serhat Koçyiğit
Abstract
Bee bread is a bee product obtained as a result of fermentation of pollen stored by honey bees in the cells of the honeycomb. Palynological analysis, chemical composition, antioxidant activity of bee bread and its cytotoxic effect against human lung carcinoma (A549), human prostate cancer (DU 145) and human neuroblastoma (SH-SY5Y) cell lines were investigated in this study. 25 plant taxa were identified with palynological analysis. Fatty acids, cyclic, aromatic, phenolic, terpenoid, diterpen and metallic complex structures were seen in GC-MS results. FTIR consequence were compatible with GC-MS results and the structure types of FTIR results were seen in the dominant compounds of GC-MS results. Radical scavenging activity (RSA) of bee bread showed inhibition variability between 20.15 ± 0.68% and 93.18 ± 0.44% depending on the concentration. In addition, the EC50 value was measured as 80.08 ± 0.10 mg/mL. Bee bread exhibited moderately cytotoxic effect at all concentrations (15.625 - 2000 µg/mL) against A549, DU 145, and SH-SY5Y cell lines. Bee bread can be used in medical fields because of it’s antioxidant and anticancer properties.
References
- Akbari, S., Abdurahman, N.H., Yunus, R.M., Alara, O.R., & Abayomi, O.O. (2019). Extraction, characterization and antioxidant activity of fenugreek (Trigonella-foenum graecum) seed oil. Materials Science for Energy Technologies, 2(2), 349-355.
- Bakour, M., Fernandes, Â., Barros, L., Sokovic, M., & Ferreira, I.C. (2019). Bee bread as a functional product: Chemical composition and bioactive properties. LWT, 109, 276-282.
- Barbarić, M., Mišković, K., Bojić, M., Lončar, M.B., Smolčić-Bubalo, A., Debeljak, Ž., & Medić-Šarić, M. (2011). Chemical composition of the ethanolic propolis extracts and its effect on HeLa cells. Journal of Ethnopharmacology, 135(3), 772-778.
- Behçet, L., & Yapar, Y. (2019). Important plants at the Matan Mountain (Bingöl/Turkey) flora with regard to beekeeping. Biological Diversity and Conservation, 12(1), 149-159.
- Bobiş, O., Mărghitaş, L.A., Dezmirean, D., Morar, O., Bonta, V., & Chirilă, F. (2010). Quality parameters and nutritional value of different commercial bee products. Bulletin UASVM Animal Science and Biotechnologies, 67, 1-2.
- Borawska, M.H., Markiewicz-Żukowska, R., Naliwajko, S.K., Moskwa, J., Bartosiuk, E., Socha, K., . . . Mariak, Z. (2014). The interaction of bee products with temozolomide in human diffuse astrocytoma, glioblastoma multiforme and astroglia cell lines. Nutrition and cancer, 66(7), 1247-1256.
- Borges, K.S., Brassesco, M.S., Scrideli, C.A., Soares, A.E.E., & Tone, L.G. (2011). Antiproliferative effects of Tubi-bee propolis in glioblastoma cell lines. Genetics and Molecular Biology, 34, 310-314.
- Chandrasekaran, M., Kannathasan, K., & Venkatesalu, V. (2008). Antimicrobial activity of fatty acid methyl esters of some members of Chenopodiaceae. Zeitschrift für Naturforschung C, 63(5-6), 331-336.
- Çakır, Y., Çobanoğlu, D.N., Dervişoğlu, G., Koçyiğit, S., Karahan, D., & Yelkovan, S. (2020). Determination Antimicrobial Activity, Palynological Characteristics and Chemical Composition of Some Honey Samples from Turkey. Mellifera, 20(1), 41-60.
- da Silva Frozza, C.O., Garcia, C.S.C., Gambato, G., de Souza, M.D.O., Salvador, M., Moura, S., . . . Borsuk, S. (2013). Chemical characterization, antioxidant and cytotoxic activities of Brazilian red propolis. Food and Chemical Toxicology, 52, 137-142.
- Ergun, M., Süslüoğlu, Z., & Bengü, A.Ş. (2017). Studying Structural Differentiation of Plant Parts of Sideritis pisidica Boiss. & Heldr. Using FTIR Spectroscopy. Türk Tarım ve Doğa Bilimleri Dergisi, 4(4), 461-467.
- Etehadpour, M., & Tavassolian, I. (2019). Ecological factors regulate essential oil yield, percent and compositions of endemic yarrow (Achillea eriophora DC.) in Southeast Iran. International Journal of Horticultural Science and Technology, 6(2), 201-215.
- Ferlay, J., Soerjomataram, I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., . . . Bray, F. (2015). Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. International journal of cancer, 136(5), E359-E386.
- Ghosh, K., & Indra, N. (2014). Phytochemistry, in vitro free radical scavenging, chelating and toxicity of Centela asiatica L.(Apiaceae) ethanolic leaf extract. International Journal of Pharmaceutical Sciences Review and Research, 29, 328-334.
- Gilliam, M. (1979). Microbiology of pollen and bee bread: the yeasts. Apidologie, 10(1), 43-53.
- Giroud, B., Vauchez, A., Vulliet, E., Wiest, L., & Buleté, A. (2013). Trace level determination of pyrethroid and neonicotinoid insecticides in beebread using acetonitrile-based extraction followed by analysis with ultra-high-performance liquid chromatography–tandem mass spectrometry. Journal of Chromatography A, 1316, 53-61.
- Greenland, G.J., & Bowden, B.F. (1994). Cembranoid diterpenes related to sarcophytol A from the soft coral Sarcophyton trocheliophorum (Alcyonacea). Australian Journal of Chemistry, 47(11), 2013-2021.
- Hatano, T., Kagawa, H., Yasuhara, T., & Okuda, T. (1988). Two new flavonoids and other constituents in licorice root: their relative astringency and radical scavenging effects. Chemical and pharmaceutical bulletin, 36(6), 2090-2097.
- Heck, J.E., Ritz, B., Hung, R.J., Hashibe, M., & Boffetta, P. (2009). The epidemiology of neuroblastoma: a review. Paediatric and perinatal epidemiology, 23(2), 125-143.
- Jemal, A., Bray, F., Center, M.M., Ferlay, J., Ward, E., & Forman, D. (2011). Global cancer statistics. CA: a cancer journal for clinicians, 61(2), 69-90.
- Kaplan, M., Karaoğlu, Ö., & Silici, S. (2019). An Evaluation on Bee Bread: Chemical and Palynological Analysis. Mellifera, 19(1), 21-29.
- Kaya, B., Darendelioğlu, E., Dervişoğlu, G., & Tartik, M. (2018). Determination of comparative biological activities of silver nanoparticles formed by biological synthesis using Achillea Vermicularis. Pak. J. Bot, 50(4), 1423-1432.
- Khan, F., Abdullah Asuhaimi, F., Jalal, T.K., Roheem, F.O., Natto, H.A., Johan, M.F., . . . Abdul Wahab, R. (2019). Hystrix Brachyura Bezoar Characterization, Antioxidant Activity Screening, and Anticancer Activity on Melanoma Cells (A375): A Preliminary Study. Antioxidants, 8(2), 39.
- Kostova, I. (2006). Ruthenium complexes as anticancer agents. Current medicinal chemistry, 13(9), 1085-1107.
- Kuptsov, A., & Zhizhin, G.N. (1998). Handbook of Fourier transform Raman and infrared spectra of polymers. Elsevier.
- Li, X., Wang, Z.G., Chen, H.H., & Liu, S.G. (2014). The antioxidant methyl 3-(3,5-di-tert-butyl-4-hydroxyphenyl)propionate. Acta Crystallogr C Struct Chem, 70(Pt 11), 1050-1053. https://doi.org/10.1107/s2053229614021445
- Liu, X.D., Zhang, F.B., Zhou, B., Shan, H., & Chen, P.Y. (2015). Effect of sonication on different quality parameters of Pinus massoniana pollen. Ultrasonics sonochemistry, 22, 174-181.
- Luz, C.F.P.D., & Barth, O.M. (2012). Pollen analysis of honey and beebread derived from Brazilian mangroves. Brazilian Journal of Botany, 35(1), 79-85.
- Magalhães, L.M., Segundo, M.A., Reis, S., & Lima, J.L. (2008). Methodological aspects about in vitro evaluation of antioxidant properties. Analytica chimica acta, 613(1), 1-19.
- Mărgăoan, R., Stranț, M., Varadi, A., Topal, E., Yücel, B., Cornea-Cipcigan, M., . . . Vodnar, D.C. (2019). Bee collected pollen and bee bread: Bioactive constituents and health benefits. Antioxidants, 8(12), 568.
- Markiewicz-Żukowska, R., Naliwajko, S.K., Bartosiuk, E., Moskwa, J., Isidorov, V., Soroczyńska, J., & Borawska, M.H. (2013). Chemical composition and antioxidant activity of beebread, and its influence on the glioblastoma cell line (U87MG). Journal of Apicultural Science, 57(2), 147-157. https://doi.org/doi:10.2478/jas-2013-0025
- Mayda, N., Özkök, A., Bayram, N.E., Gerçek, Y.C., & Sorkun, K. (2020). Bee bread and bee pollen of different plant sources: Determination of phenolic content, antioxidant activity, fatty acid and element profiles. Journal of Food Measurement and Characterization, 14(4), 1795-1809.
- Pinto, M.E., Araujo, S.G., Morais, M.I., Sá, N.P., Lima, C.M., Rosa, C.A., . . . Lima, L.A. (2017). Antifungal and antioxidant activity of fatty acid methyl esters from vegetable oils. Anais da Academia Brasileira de Ciências, 89, 1671-1681.
- Reedijk, B.J. (2008). Metal-ligand exchange kinetics in platinum and ruthenium complexes. Platinum Metals Review, 52(1), 2-11.
- Sobral, F., Calhelha, R.C., Barros, L., Dueñas, M., Tomás, A., Santos-Buelga, C., . . . Ferreira, I.C. (2017). Flavonoid composition and antitumor activity of bee bread collected in northeast Portugal. Molecules, 22(2), 248.
- Soumya, V., Muzib, Y.I., Venkatesh, P., & Hariprasath, K. (2014). GC-MS analysis of Cocus nucifera flower extract and its effects on heterogeneous symptoms of polycystic ovarian disease in female Wistar rats. Chinese journal of natural medicines, 12(9), 677-684.
- Sreeramulu, D., Reddy, C., Chauhan, A., Balakrishna, N., & Raghunath, M. (2013). Natural antioxidant activity of commonly consumed plant foods in India: effect of domestic processing. Oxidative Medicine and Cellular Longevity, 2013.
- Syamdidi, H.E.I., & Irianto, G. (2016). Agar-abundant Marine Carbohydrate from Seaweeds in Indonesia: Production, Bioactivity, and Utilization. In Marine Glycobiology (pp. 275-282). CRC Press.
- Tuzcu, Z., Koclar, G., Agca, C.A., Aykutoglu, G., Dervisoglu, G., Tartik, M., . . . Sahin, K. (2017). Antioxidant, antimicrobial and anticancer effects of different extracts from wild edible plant Eremurus spectabilis leaves and roots. International journal of clinical and experimental medicine, 10(3), 4787-4797.
- Wróblewska, A., Warakomska, Z., & Koter, M. (2006). Pollen analysis of bee products from the north-eastern Poland. Journal of Apicultural Science, 50(1), 71-83.
- Yang, X., Guo, D., Zhang, J., & Wu, M. (2007). Characterization and anti-tumor activity of pollen polysaccharide. International immunopharmacology, 7(3), 401-408.