PHYTOCHEMICAL SCREENING, ANTIOXIDANT AND ANTI-INFLAMMATORY PROPERTIES OF SEVERAL STINGLESS BEE POLLENS PROCESSED USING DIFFERENT DRYING METHODS
Year 2023,
, 153 - 166, 19.11.2023
Netty Maria Naıbaho
,
Widya Fatrıasarı
Irawan Wijaya Kusuma
Enos Tangke Arung
Abstract
Antioxidants play a crucial function in fighting free radicals that can harm biomolecules in the human body and damage cells, which can lead to immunological disorders including inflammation. In this research, we evaluated bee pollen extracts from six stingless bees (Heterotrigona itama, Tetragonula reepeni, Tetragonula testaceitarsis, Tetragonula fuscobalteata, Tetragonula iridipennis, and Tetragonula pagdeni) processed using different drying methods for antioxidant and anti-inflammatory activity. Each sample was divided into two specimens, where one was processed by ovendrying at 40ºC and the second was chilled at 4 ºC, then extracted by ethanol. The extracts of T. fuscobalteata had the highest antioxidant activity when dried in an oven with an IC50 value of 36.47 µg/mL, while T. reepeni using a chiller was 41.30 mg/mL. The highest anti-inflammatory activity was for oven-dried T. fuscobalteata with an IC50 of 39.70 mg/mL, while chilled T. reepeni was 34.30 µg/mL. Different drying techniques can affect the antioxidant and anti-inflammatory activity of bee pollen extracts as well as their potential as food, pharmaceutical and cosmetic ingredients.
Supporting Institution
The Ministry of Education, Culture, Research and Technology, the Republic of Indonesia and National Research and Innovation Agency (BRIN)
Project Number
Grant no 429/UN17.L1/HK/2022 and 398/II/FR/3/2022
Thanks
The Ministry of Education, Culture, Research and Technology, the Republic of Indonesia in the scheme Doctoral Dissertation Research 2022 (Grant no 429/UN17.L1/HK/2022) and by the Deputy of Research and Innovation, National Research and Innovation Agency (BRIN) with Grant number: 398/II/FR/3/2022.
References
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- Anjos, Ofélia VP, Delgado T, Estevinho L. Influence of the storage conditions on the quality of bee pollen. Zemdirbyste-Agriculture, 2019;106(1):87–94, doi:10.13080/z-a.2019.106.012
- AOAC. Official Methods of Analysis of the Association of Official Analytical Chemists. Marlyand: the Association of Official Analytical Chemists, 2006.
- Arung ET, Shimizu K, Kondo R. Inhibitory effect of isoprenoid-substituted flavonoids isolated from Artocarpus heterophyllus on melanin biosynthesis. Planta Med, 2008;72(9):847–850. https://doi.org/10.1055/s-2006-931606
- Arung ET, Ramadhan R, Khairunnisa B, Amen Y, Matsumoto M, Nagata M, Wijaya IK, et al. Cytotoxicity effect of honey, bee pollen, and propolis from seven stingless bees in some cancer cell lines. Saudi Journal of Biological Sciences, 2021;28:7182-7189. https://doi.org/10.1016/j.sjbs.2021.08.017
- Bai R, Yao C, Zhong Z, Ge J, Bai Z, Ye X, Xie T, Xie Y. Discovery of natural anti-inflammatory alkaloids: Potential leads for the drug discovery for the treatment of inflammation. European Journal of Medicinal Chemistry, 2021;213:18–22 https://doi.org/10.1016/j.ejmech.2021.113165
- Bansal Y, Sethi P, Bansal G. Coumarin: a potential nucleus for anti-inflammatory molecules. Med Chem Res, 2012;1-12. doi:DOI 10.1007/s00044-012-0321-6
- Barajas J, Cortes-Rodriguez M, Sandova R. Effect of temperature on the drying process of bee pollen from two zones of Colombia. Journal of Food Process Engineering, 2012;35:134–148
- Campos MGR, Bogdanov S, Almeida-Muradian LB, Szczesna T, Mancebo Y, Frigerio C, Ferreira F. Pollen composition and standardisation of analytical methods. Journal of Apicultural Research, 2015;47(2):154–161.http://dx.doi.org/10.1080/00218839.2008.11101443
- Castagna A, Benelli G, Conte G, Sgherri C, Signorini F, Nicolella C, Ranieri A, Canale A. Drying Techniques and Storage: Do They Affect the Nutritional Value of Bee-Collected Pollen? Molecules, 2020;25:4925. http://dx.doi.org/10.3390/molecules25214925
- Cinkmanis I, Dimins F, Mikelsone V. Influence of Lyophilization and convective type drying. Foodbalt, 2017;201-203. doi:10.22616/foodbalt.2017.038
- Denisow B, Denisow-Pietrzyk M. Biological and therapeutic properties of bee pollen: a review. Journal Science Food Agric, 2016:1–8. doi:10.1002/jsfa.7729
- Dias LG, Tolentino G, Pascoal A, Estevinho LM. Effect of processing conditions on the bioactive compounds and biological properties of bee pollen. Journal of Apicultural Research, 2016;55(5):357–365. http://dx.doi.org/10.1080/00218839.2016.1248109
- Diaz P, Chul SJ, Lee S, Khoo C, Rao SK. Antioxidant and anti-inflammatory activities of selected medicinal plants and fungi containing phenolic and flavonoid compounds. Chinese Medicine, 2012;7(26):2–9. http://www.cmjournal.org/content/7/1/26
- Fuenmayor C, Zuluaga CD, Díaz MC, Quicazán CM, Cosio M, Mannino S. Evaluation of the physicochemical and functional properties of Colombian bee pollen. Rev MVZ Córdob, 2014;19(1):4003–4014. https://revistamvz.unicordoba.edu.co/article/view/120/189
- Harbone JB. Metode Fitokimia (Terjemahan). 2. Bandung: ITB Bandung, 1987
- Hassan A, Akmal Z, Khan N. The Phytochemical Screening and Antioxidants Potential of Schoenoplectus triqueter L. Palla. Journal of Chemistry, 2020:1–8. doi:https://doi.org/10.1155/2020/3865139
- Isik A, Ozdemir M, Doymaz I. Effect of hot air drying on quality characteristics and physicochemical properties of bee pollen. Food Science and Technology, 2018;1-9. https://doi.org/10.1590/fst.02818
- Kahraman HA, Tutun H, Kaya MM, Usluer MS, Tutun S, Yaman C, Sevin S, Keyvan E. Ethanolic extract of Turkish bee pollen and propolis: phenolic composition, antiradical, antiproliferative and antibacterial activities. Biotechnology & Biotechnological Equipment, 2022;36(1):45–56 https://doi.org/10.1080/13102818.2022.2045217
- Kalaycıoglu Z, Kaygusuz H, Doker S, Kolaylı S, Erim FB. Characterization of Turkish honeybee pollens by principal component analysis based on their individual organic acids, sugars, minerals, and antioxidant activities. LWT – Food Science and Technology, 2017;84:402–408. http://dx.doi.org/10.1016/j.lwt.2017.06.003
- Kocot J, Małgorzata K, Luchowska-Kocot D, Kurzepa J, Musik I. Antioxidant Potential of Propolis, Bee Pollen, and Royal Jelly: Possible Medical Application, Oxidative Medicine and Cellular Longevity, 2018;29:29. https://doi.org/10.1155/2018/7074209
- Kokate CK. Pharmacognosy. 16. Mumbai: Niali Prakasham, 2001
- Lopes AJO, Vasconcelos CC, Garcia JBS, Pinheiro MSD, Pereira FAN, Camelo DS , Morais SV, et al. Anti‐Inflammatory and Antioxidant Activity of Pollen Extract Collected by Scaptotrigona affinis postica: in silico, in vitro, and in vivo Studies. Antioxidant MDPI, 2020;9 (103):1–16. doi:10.3390/antiox9020103
- Martemucci G, Costagliola C, Mariano M, Andrea L, Napolitano P, D’Alessandro AG. Free Radical Properties, Source and Targets, Antioxidant Consumption and Health. Oxygen, 2022;2: 48–78. https://doi.org/10.3390/oxygen2020006
- Minarti S, Junus M, Radiati LE, Jaya F, Fa'izah S, Landa F, Handayani I, Warasi DM, Fitriyono MA. Drying Methods Effect on Chemical Content of Pollen Study of Oil Palm Pollen as Honeybee Feed. Proceedings of the International Conference on Improving Tropical Animal Production for Food Security (ITAPS 2021). Atlantis Press International, 2022;502–505
- Mohammad SM, Mahmud-Ab-Rashid NK, Zawawi N. Stingless Bee-Collected Pollen (Bee Bread): Chemical and Microbiology Properties and Health Benefits. Molecules, 2021;26 (957):1–29 https://doi.org/10.3390/molecules26040957
- Oyedapo O, Akinpelu B, Akinwunmi K, Adeyinka M, Sipeolu F. Red blood cell membrane stabilizing potentials. International Journal of Plant Physiology and Biochemistry, 2010;2: 46–5. http://www.academicjournals.org/ijppb
- Özcan MM, Aljuhaim F, Babiker EE, Uslu N, Ceylan DA, Ghafoor K, Mete MÖ, et al. Determination of antioxidant activity, phenolic compound, mineral contents and fatty acid compositions of bee pollen grains collected from different locations. J. Apic. Sci, 2019;63:69–79. doi:10.2478/JAS-2019-0004
- Ranieri A, Benelli G, Castagna A, Sgherri C, Signorini F, Bientinesi M, Nicolella C, Canale A. Freeze-drying duration influences the amino acid and rutin content in honeybee-collected chestnut pollen. Saudi Journal of Biological Sciences, 2017;26(2):252–255. https://doi.org/10.1016/j.sjbs.2017.08.011
- Rao GHR. Metabolic Disease Pandemic: Call for Action. EC Endocrinology and Metabolic Research, 2020;5(9):1–3
- Rzepecka-Stojko A, Drzal A, Stojko J, Buszman E. Effect of storage conditions on antioxidant activity of bee pollen extracts. Med. Weter, 2014;70(12):740–744
- Saral Ö, Kilicarslan M, Sahin H, Yildiz O, Dincer B. Evaluation of antioxidant activity of bee products of different bee races in Turkey. Turkish Journal of Veterinary and Animal Sciences, 2019;43:41–447. doi:10.3906/vet-1901-3
- Sari AM, Rosamah E, Suwinarti W, Kusuma IW, Arung ET. Aktivitas antioksidan dan antibakteri dari ekstrak bee pollen lebah kelulut (Tetragonula sarawakensis). Jurnal Riset Industri Hasil Hutan, 2021;13(2):123–132. http://dx.doi.org/10.24111/jrihh.v13i2.7050
- Senthilmurugan G, Vasanthe VB, Suresh K. Screening and antibacterial activity analysis of some important medicinal plants. International Journal of Innovation and Applied Studies, 2013;2(2):146–152. http://www.issr-journals.org/ijias/
- Singh H, Sarkar BK, Arya JC, Pal S, Kumar R, Gupta V, Singh R, Verma SC. Phytochemical and Anti-Inflammatory Evaluation of Herbal Gel Prepared from Bark Extract of Mesua Ferrea Linn. Journal of Drug Delivery and Therapeutics, 2019;9(5-s):53–56. http://dx.doi.org/10.22270/jddt.v9i5-s.3638
- Spulber S, Raciti M, Dulko-Smith B, Lupu D, Rüegg J, Nam K, Ceccatelli S. Methylmercury interferes with glucocorticoid receptor: Potential role in the mediation of developmental neurotoxicity. Toxicology and Applied Pharmacology, 2018;1–7. https://doi.org/10.1016/j.taap.2018.02.021
- Sukandar D, Nurbayt S, Rudiana T, Husna TW. Isolation and Structure Determination of Antioxidants Active Compounds from Ethyl Acetate Extract of Heartwood Namnam (Cynometra cauliflora L.).
- Kimia Terap. Indonesia, 2017;19(1):11–17. http://inajac.lipi.go.id
- Tutun H, Kaya MM, Usluer MS, Kahraman HA. Bee Pollen: Its Antioxidant Activity. U. Arı D. – U. Bee J, 2021;21(1):119–131. doi: 10.31467/uluaricilik.896045
PHYTOCHEMICAL SCREENING, ANTIOXIDANT AND ANTI-INFLAMMATORY PROPERTIES OF SEVERAL STINGLESS BEE POLLENS PROCESSED USING DIFFERENT DRYING METHODS
Year 2023,
, 153 - 166, 19.11.2023
Netty Maria Naıbaho
,
Widya Fatrıasarı
Irawan Wijaya Kusuma
Enos Tangke Arung
Abstract
Antioxidants play a crucial function in fighting free radicals that can harm biomolecules in the human body and damage cells, which can lead to immunological disorders including inflammation. In this research, we evaluated bee pollen extracts from six stingless bees (Heterotrigona itama, Tetragonula reepeni, Tetragonula testaceitarsis, Tetragonula fuscobalteata, Tetragonula iridipennis, and Tetragonula pagdeni) processed using different drying methods for antioxidant and anti-inflammatory activity. Each sample was divided into two specimens, where one was processed by ovendrying at 40ºC and the second was chilled at 4 ºC, then extracted by ethanol. The extracts of T. fuscobalteata had the highest antioxidant activity when dried in an oven with an IC50 value of 36.47 µg/mL, while T. reepeni using a chiller was 41.30 mg/mL. The highest anti-inflammatory activity was for oven-dried T. fuscobalteata with an IC50 of 39.70 mg/mL, while chilled T. reepeni was 34.30 µg/mL. Different drying techniques can affect the antioxidant and anti-inflammatory activity of bee pollen extracts as well as their potential as food, pharmaceutical and cosmetic ingredients.
Project Number
Grant no 429/UN17.L1/HK/2022 and 398/II/FR/3/2022
References
- Almeida-Muradian LB, Pamplona LC, Coimbra S, Barth OM. Chemical composition and botanical evaluation of dried bee pollen pellets. Journal of Food Composition and Analysis, 2005;18(1):105–111. doi:https://doi.org/10.1016/j.jfca.2003.10.008
- Anjos, Ofélia VP, Delgado T, Estevinho L. Influence of the storage conditions on the quality of bee pollen. Zemdirbyste-Agriculture, 2019;106(1):87–94, doi:10.13080/z-a.2019.106.012
- AOAC. Official Methods of Analysis of the Association of Official Analytical Chemists. Marlyand: the Association of Official Analytical Chemists, 2006.
- Arung ET, Shimizu K, Kondo R. Inhibitory effect of isoprenoid-substituted flavonoids isolated from Artocarpus heterophyllus on melanin biosynthesis. Planta Med, 2008;72(9):847–850. https://doi.org/10.1055/s-2006-931606
- Arung ET, Ramadhan R, Khairunnisa B, Amen Y, Matsumoto M, Nagata M, Wijaya IK, et al. Cytotoxicity effect of honey, bee pollen, and propolis from seven stingless bees in some cancer cell lines. Saudi Journal of Biological Sciences, 2021;28:7182-7189. https://doi.org/10.1016/j.sjbs.2021.08.017
- Bai R, Yao C, Zhong Z, Ge J, Bai Z, Ye X, Xie T, Xie Y. Discovery of natural anti-inflammatory alkaloids: Potential leads for the drug discovery for the treatment of inflammation. European Journal of Medicinal Chemistry, 2021;213:18–22 https://doi.org/10.1016/j.ejmech.2021.113165
- Bansal Y, Sethi P, Bansal G. Coumarin: a potential nucleus for anti-inflammatory molecules. Med Chem Res, 2012;1-12. doi:DOI 10.1007/s00044-012-0321-6
- Barajas J, Cortes-Rodriguez M, Sandova R. Effect of temperature on the drying process of bee pollen from two zones of Colombia. Journal of Food Process Engineering, 2012;35:134–148
- Campos MGR, Bogdanov S, Almeida-Muradian LB, Szczesna T, Mancebo Y, Frigerio C, Ferreira F. Pollen composition and standardisation of analytical methods. Journal of Apicultural Research, 2015;47(2):154–161.http://dx.doi.org/10.1080/00218839.2008.11101443
- Castagna A, Benelli G, Conte G, Sgherri C, Signorini F, Nicolella C, Ranieri A, Canale A. Drying Techniques and Storage: Do They Affect the Nutritional Value of Bee-Collected Pollen? Molecules, 2020;25:4925. http://dx.doi.org/10.3390/molecules25214925
- Cinkmanis I, Dimins F, Mikelsone V. Influence of Lyophilization and convective type drying. Foodbalt, 2017;201-203. doi:10.22616/foodbalt.2017.038
- Denisow B, Denisow-Pietrzyk M. Biological and therapeutic properties of bee pollen: a review. Journal Science Food Agric, 2016:1–8. doi:10.1002/jsfa.7729
- Dias LG, Tolentino G, Pascoal A, Estevinho LM. Effect of processing conditions on the bioactive compounds and biological properties of bee pollen. Journal of Apicultural Research, 2016;55(5):357–365. http://dx.doi.org/10.1080/00218839.2016.1248109
- Diaz P, Chul SJ, Lee S, Khoo C, Rao SK. Antioxidant and anti-inflammatory activities of selected medicinal plants and fungi containing phenolic and flavonoid compounds. Chinese Medicine, 2012;7(26):2–9. http://www.cmjournal.org/content/7/1/26
- Fuenmayor C, Zuluaga CD, Díaz MC, Quicazán CM, Cosio M, Mannino S. Evaluation of the physicochemical and functional properties of Colombian bee pollen. Rev MVZ Córdob, 2014;19(1):4003–4014. https://revistamvz.unicordoba.edu.co/article/view/120/189
- Harbone JB. Metode Fitokimia (Terjemahan). 2. Bandung: ITB Bandung, 1987
- Hassan A, Akmal Z, Khan N. The Phytochemical Screening and Antioxidants Potential of Schoenoplectus triqueter L. Palla. Journal of Chemistry, 2020:1–8. doi:https://doi.org/10.1155/2020/3865139
- Isik A, Ozdemir M, Doymaz I. Effect of hot air drying on quality characteristics and physicochemical properties of bee pollen. Food Science and Technology, 2018;1-9. https://doi.org/10.1590/fst.02818
- Kahraman HA, Tutun H, Kaya MM, Usluer MS, Tutun S, Yaman C, Sevin S, Keyvan E. Ethanolic extract of Turkish bee pollen and propolis: phenolic composition, antiradical, antiproliferative and antibacterial activities. Biotechnology & Biotechnological Equipment, 2022;36(1):45–56 https://doi.org/10.1080/13102818.2022.2045217
- Kalaycıoglu Z, Kaygusuz H, Doker S, Kolaylı S, Erim FB. Characterization of Turkish honeybee pollens by principal component analysis based on their individual organic acids, sugars, minerals, and antioxidant activities. LWT – Food Science and Technology, 2017;84:402–408. http://dx.doi.org/10.1016/j.lwt.2017.06.003
- Kocot J, Małgorzata K, Luchowska-Kocot D, Kurzepa J, Musik I. Antioxidant Potential of Propolis, Bee Pollen, and Royal Jelly: Possible Medical Application, Oxidative Medicine and Cellular Longevity, 2018;29:29. https://doi.org/10.1155/2018/7074209
- Kokate CK. Pharmacognosy. 16. Mumbai: Niali Prakasham, 2001
- Lopes AJO, Vasconcelos CC, Garcia JBS, Pinheiro MSD, Pereira FAN, Camelo DS , Morais SV, et al. Anti‐Inflammatory and Antioxidant Activity of Pollen Extract Collected by Scaptotrigona affinis postica: in silico, in vitro, and in vivo Studies. Antioxidant MDPI, 2020;9 (103):1–16. doi:10.3390/antiox9020103
- Martemucci G, Costagliola C, Mariano M, Andrea L, Napolitano P, D’Alessandro AG. Free Radical Properties, Source and Targets, Antioxidant Consumption and Health. Oxygen, 2022;2: 48–78. https://doi.org/10.3390/oxygen2020006
- Minarti S, Junus M, Radiati LE, Jaya F, Fa'izah S, Landa F, Handayani I, Warasi DM, Fitriyono MA. Drying Methods Effect on Chemical Content of Pollen Study of Oil Palm Pollen as Honeybee Feed. Proceedings of the International Conference on Improving Tropical Animal Production for Food Security (ITAPS 2021). Atlantis Press International, 2022;502–505
- Mohammad SM, Mahmud-Ab-Rashid NK, Zawawi N. Stingless Bee-Collected Pollen (Bee Bread): Chemical and Microbiology Properties and Health Benefits. Molecules, 2021;26 (957):1–29 https://doi.org/10.3390/molecules26040957
- Oyedapo O, Akinpelu B, Akinwunmi K, Adeyinka M, Sipeolu F. Red blood cell membrane stabilizing potentials. International Journal of Plant Physiology and Biochemistry, 2010;2: 46–5. http://www.academicjournals.org/ijppb
- Özcan MM, Aljuhaim F, Babiker EE, Uslu N, Ceylan DA, Ghafoor K, Mete MÖ, et al. Determination of antioxidant activity, phenolic compound, mineral contents and fatty acid compositions of bee pollen grains collected from different locations. J. Apic. Sci, 2019;63:69–79. doi:10.2478/JAS-2019-0004
- Ranieri A, Benelli G, Castagna A, Sgherri C, Signorini F, Bientinesi M, Nicolella C, Canale A. Freeze-drying duration influences the amino acid and rutin content in honeybee-collected chestnut pollen. Saudi Journal of Biological Sciences, 2017;26(2):252–255. https://doi.org/10.1016/j.sjbs.2017.08.011
- Rao GHR. Metabolic Disease Pandemic: Call for Action. EC Endocrinology and Metabolic Research, 2020;5(9):1–3
- Rzepecka-Stojko A, Drzal A, Stojko J, Buszman E. Effect of storage conditions on antioxidant activity of bee pollen extracts. Med. Weter, 2014;70(12):740–744
- Saral Ö, Kilicarslan M, Sahin H, Yildiz O, Dincer B. Evaluation of antioxidant activity of bee products of different bee races in Turkey. Turkish Journal of Veterinary and Animal Sciences, 2019;43:41–447. doi:10.3906/vet-1901-3
- Sari AM, Rosamah E, Suwinarti W, Kusuma IW, Arung ET. Aktivitas antioksidan dan antibakteri dari ekstrak bee pollen lebah kelulut (Tetragonula sarawakensis). Jurnal Riset Industri Hasil Hutan, 2021;13(2):123–132. http://dx.doi.org/10.24111/jrihh.v13i2.7050
- Senthilmurugan G, Vasanthe VB, Suresh K. Screening and antibacterial activity analysis of some important medicinal plants. International Journal of Innovation and Applied Studies, 2013;2(2):146–152. http://www.issr-journals.org/ijias/
- Singh H, Sarkar BK, Arya JC, Pal S, Kumar R, Gupta V, Singh R, Verma SC. Phytochemical and Anti-Inflammatory Evaluation of Herbal Gel Prepared from Bark Extract of Mesua Ferrea Linn. Journal of Drug Delivery and Therapeutics, 2019;9(5-s):53–56. http://dx.doi.org/10.22270/jddt.v9i5-s.3638
- Spulber S, Raciti M, Dulko-Smith B, Lupu D, Rüegg J, Nam K, Ceccatelli S. Methylmercury interferes with glucocorticoid receptor: Potential role in the mediation of developmental neurotoxicity. Toxicology and Applied Pharmacology, 2018;1–7. https://doi.org/10.1016/j.taap.2018.02.021
- Sukandar D, Nurbayt S, Rudiana T, Husna TW. Isolation and Structure Determination of Antioxidants Active Compounds from Ethyl Acetate Extract of Heartwood Namnam (Cynometra cauliflora L.).
- Kimia Terap. Indonesia, 2017;19(1):11–17. http://inajac.lipi.go.id
- Tutun H, Kaya MM, Usluer MS, Kahraman HA. Bee Pollen: Its Antioxidant Activity. U. Arı D. – U. Bee J, 2021;21(1):119–131. doi: 10.31467/uluaricilik.896045