Content and Antimicrobial Activities of Bingol Royal Jelly
Year 2020,
Volume: 7 Issue: 2, 480 - 486, 24.04.2020
A. Şükrü Bengü
,
Adnan Ayna
Sedanur Özbolat
Abdullah Tunç
,
Gürkan Aykutoğlu
,
Mehmet Çiftci
Ekrem Darendelioğlu
Abstract
Royal jelly (RJ) is the special nutriment of the larva of queen honeybee (Apis mellifera) which is composed of several bioactive substances that include amino acids, proteins, carbohydrates, lipids, mineral salts, and vitamins. The content of RJ varies depending on genotype of the bees according to the flora species and climatic conditions and this affects biological activities of RJ. In recent years, literature has perceived an exponential growth in amount of drug (antibiotic)-resistant pathogenic bacteria. The main reasons of growing antibiotic resistance might be credited to the abuse of the antibiotic usage demonstrating prominence of examining other choices other than the communal antibiotics, such as bee products), to avoid a additional build-up in antibiotic resistance. To our knowledge, chemical content and antimicrobial activity of Bingol RJ (BRJ) has not been investigated to date. Therefore, the purpose of this study was to study composition and antimicrobial activities of BRJ. The results demonstrated that BRJ contains major flavonoids and phenolics such as apigenin, quercetin, naringenin, gallic acid, caffeic acid that contribute antimicrobial and antioxidant properties of BRJ. We have also shown that there are some middle and short chain fatty acids that include Linoleic acid and Propionic acid. BRJ also contain majority of trace elements and mineral. In addition to chemical content, antimicrobial activity of BRJ was also investigated towards pathogens. BRJ showed antimicrobial activity against Salmonella typhimurium (8.64 mm), Escherichia coli (9.1 mm) and Staphylococcus aureus (10.73 mm).
Thanks
This study was financially supported by Presidency of The Republic of Turkey Strategy and Budget Presidency (Former Development Ministry), coordinated by Council of Higher Education and organized by The Scientific Research Projects Coordination Unit of Bingol University (Project Number: 2017K124000-BÜBAP-PİKOM-Arı.2018.001).
References
- Al-Abbadi, A.A. 2019. The Antimicrobial Potential of Royal Jelly against some Pathogenic Bacteria and Fungi. Jordan Journal of Biological Sciences, 12(4):445-451.
- Arshi, A., Jafari, M., Sadeghi, A., Gholami, M., Kabiri, H. and Abolhasani, M. 2019. Chrysin and its relation with gastric cancer. Journal of BioScience and Biotechnology, 8(1): 17-24.
- Asadi, N., Kheradmand, A., Gholami, M., Saidi, S.H. and Mirhadi, S.A. 2019. Effect of royal jelly on testicular antioxidant enzymes activity, MDA level and spermatogenesis in rat experimental Varicocele model. Tissue and Cell, 57: 70-77.
- Bărnuţiu, L.I., Mărghitaş, L.A., Dezmirean, D.S., Mihai, C.M. and Bobiş, O. 2011. Chemical composition and antimicrobial activity of Royal Jelly-REVIEW. Scientific Papers Animal Science and Biotechnologies, 44(2): 67-72.
- Basile, A., Giordano, S., López-Sáez, J.A. and Cobianchi, R.C. 1999. Antibacterial activity of pure flavonoids isolated from mosses. Phytochemistry, 52(8), 1479-1482.
- Caglayan, C., Kandemir, F.M., Yildirim, S., Kucukler, S. and Eser, G. 2019. Rutin protects mercuric chloride‐induced nephrotoxicity via targeting of aquaporin 1 level, oxidative stress, apoptosis and inflammation in rats. Journal of Trace Elements in Medicine and Biology, 54: 69-78.
- Chanwitheesuk, A., Teerawutgulrag, A., Kilburn, J.D. and Rakariyatham, N. 2007. Antimicrobial gallic acid from Caesalpinia mimosoides Lamk. Food Chemistry, 100(3): 1044-1048.
- Cornara, L., Biagi, M., Xiao, J. and Burlando, B. 2017. Therapeutic properties of bioactive compounds from different honeybee products. Frontiers in pharmacology, 8: 412-432.
- Coutinho, D., Karibasappa, S. N., & Mehta, D. S. 2018. Royal Jelly Antimicrobial Activity against Periodontopathic Bacteria. Journal of Interdisciplinary Dentistry, 8(1), 18-22.
- Danis, T.C.P., Madeira, V.M.C. and Almeida, M.L.M. 1994. Action of phenolic derivates (acetoaminophen, salycilate and 5-amino salycilate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Archives of Biochemistry and Biophysics, 315: 161-9.
- Demirel Sezer, E., Oktay, L.M., Karadadaş, E., Memmedov, H., Selvi Gunel, N. and Sözmen, E. 2019. Assessing Anticancer Potential of Blueberry Flavonoids, Quercetin, Kaempferol, and Gentisic Acid, Through Oxidative Stress and Apoptosis Parameters on HCT-116 Cells. Journal of medicinal food, 22(11): 1-9.
- Filipič, B., Gradišnik, L., Rihar, K., Šooš, E., Pereyra, A. and Potokar, J. 2015. The influence of royal jelly and human interferon-alpha (HuIFN-αN3) on proliferation, glutathione level and lipid peroxidation in human colorectal adenocarcinoma cells in vitro. Arhiv za higijenu rada i toksikologiju, 66(4): 0-0.
- Fratini, F., Cilia, G., Mancini, S. and Felicioli, A. 2016. Royal Jelly: An ancient remedy with remarkable antibacterial properties. Microbiological Research, 192: 130-141.
- Gu, H., Song, I.B., Han, H.J., Lee, N.Y., Cha, J.Y., Son, Y.K. and Kwon, J. 2018. Antioxidant Activity of Royal Jelly Hydrolysates Obtained by Enzymatic Treatment. Korean journal for food science of animal resources, 38(1): 135-142.
- Imran, M., Salehi, B., Sharifi-Rad, J., Aslam Gondal, T., Saeed, F., Imran, A., ... and Guerreiro, S.G. 2019. Kaempferol: A Key Emphasis to Its Anticancer Potential. Molecules, 24(12): 2277.
- Kaya, B., Darendelioğlu, E., Dervişoğlu, G., and 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.
- Khazaei, M. R., Makalani, F., Ghanbari, E., Fayzemahdavi, M. and Khazaei, M. 2018. An overview of effective herbal and antioxidant compounds on diabetes. Journal of Contemporary Medical Sciences, 4(3):126-133.
- 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. Oxidative medicine and cellular longevity, 1-29.
- López-Gutiérrez, N., del Mar Aguilera-Luiz, M., Romero-González, R., Vidal, J.L.M. and Frenich, A.G. 2014. Fast analysis of polyphenols in royal jelly products using automated TurboFlow™-liquid chromatography–Orbitrap high resolution mass spectrometry. Journal of Chromatography B, 973: 17-28.
Nabas, Z., Haddadin, M.S.Y., Haddadin, J. and Nazer, I.K. 2014. Chemical composition of royal jelly and effects of synbiotic with two different locally isolated probiotic strains on antioxidant activities. Polish Journal of Food and Nutrition Sciences, 64(3): 171-180.
- Nagai, T. and Inoue, R. 2004. Preparation and the functional properties of water extract and alkaline extract of royal jelly. Food chemistry, 84(2): 181-186.
- Nitiema, L. W., Savadogo, A., Simpore, J., Dianou, D. and Traore, A.S. 2012. In vitro antimicrobial activity of some phenolic compounds (coumarin and quercetin) against gastroenteritis bacterial strains. International Journal of Microbiology Research, 3(3): 183-187.
- Noori, A.L., Al Ghamdi, A., Ansari, M.J., Al-Attal, Y., Al-Mubarak, A. and Salom, K. 2013. Differences in composition of honey samples and their impact on the antimicrobial activities against drug multiresistant bacteria and pathogenic fungi. Archives of medical research, 44(4), 307-316.
- Nugent, R., Back, E. and Beith, A. 2010. The race against drug resistance. Washington (DC): Center for Global Development.
- Park, H.M., Cho, M.H., Cho, Y. and Kim, S.Y. 2012. Royal jelly increases collagen production in rat skin after ovariectomy. Journal of medicinal food, 15(6): 568-575.
- Park, H.G., Kim, B.Y., Park, M.J., Deng, Y., Choi, Y.S., Lee, K.S. and Jin, B.R. 2019. Antibacterial activity of major royal jelly proteins of the honeybee (Apis mellifera) royal jelly. Journal of Asia-Pacific Entomology.
- Pavel, C. I., Mărghitaş, L.A., Bobiş, O., Dezmirean, D.S., Şapcaliu, A., Radoi, I. and Mădaş, M.N. 2011. Biological activities of royal jelly-review. Scientific Papers Animal Science and Biotechnologies, 44(2): 108-118.
- Prieto, P., Pineda, M. and Aguilar, M. 1999. Spectrophotometric Quantitation of Antioxidant Capacity through the Formation of a Phosphomolybdenum Complex: Specific Application to the Determination of Vitamin E. Analytical Biochemistry, 269: 337-341.
- Ruch, R.J., Cheng, S.J. and Klaunig, J.E. 1989. Prevention of cytotoxicity and inhibition of intercellular communication by antioxidant catechins isolated from chinese green tea. Carcinogenesis, 10(6): 1003-1008.
- Šedivá, M., Laho, M., Kohútová, L., Mojžišová, A., Majtán, J. and Klaudiny, J. 2018. 10-HDA, A Major Fatty Acid of Royal Jelly, Exhibits pH Dependent Growth-Inhibitory Activity Against Different Strains of Paenibacillus larvae. Molecules, 23(12): 32-36.
- Stocker, A., Schramel, P., Kettrup, A. and Bengsch, E. 2005. Trace and mineral elements in royal jelly and homeostatic effects. Journal of Trace Elements in Medicine and Biology, 19:(2-3), 183-189.
- Taslimi, P., Kandemir, F.M., Demir, Y., İleritürk, M., Temel, Y., Caglayan, C. and Gulçin, İ. 2019. The antidiabetic and anticholinergic effects of chrysin on cyclophosphamide‐induced multiple organ toxicity in rats: Pharmacological evaluation of some metabolic enzyme activities. Journal of biochemical and molecular toxicology, e22313.
- Turk, E., Kandemir, F.M., Yildirim, S., Caglayan, C., Kucukler, S. and Kuzu, M. 2019. Protective effect of hesperidin on sodium arsenite-induced nephrotoxicity and hepatotoxicity in rats. Biological trace element research, 189(1): 95-108.
- Wang, B., Li, L., Fu, J., Yu, P., Gong, D., Zeng, C. And Zeng, Z. 2016. Effects of long‐chain and medium‐chain fatty acids on apoptosis and oxidative stress in human liver cells with steatosis. Journal of food science, 81(3): 794-800.
- WHO. World Health Organization. 2012. Antimicrobial Resistance. World Health Organization. Geneva.
- Yang, Y.C., Chou, W.M., Widowati, D.A., Lin, I.P. and Peng, C.C. 2018. 10-hydroxy-2-decenoic acid of royal jelly exhibits bactericide and anti-inflammatory activity in human colon cancer cells. BMC complementary and alternative medicine, 18(1):202-207.
- Yang, X., Li, Y., Wang, L., Li, L., Guo, L., Huang, F. and Zhao, H. 2019. Determination of 10‐Hydroxy‐2‐Decenoic Acid of Royal Jelly Using Near‐Infrared Spectroscopy Combined with Chemometrics. Journal of food science.
Bingöl Arı Sütünün İçeriği ve Antimikrobiyal Aktivitesi
Year 2020,
Volume: 7 Issue: 2, 480 - 486, 24.04.2020
A. Şükrü Bengü
,
Adnan Ayna
Sedanur Özbolat
Abdullah Tunç
,
Gürkan Aykutoğlu
,
Mehmet Çiftci
Ekrem Darendelioğlu
Abstract
Arı sütü (AS), amino asitler, proteinler, karbohidratlar, lipitler, mineral tuzları ve vitaminleri içeren çeşitli biyoaktif maddelerden oluşan kraliçe bal arısı larvalarının (Apis mellifera) özel besleyicisidir. AS içeriği, flora türlerine ve iklim koşullarına göre arıların genotipine bağlı olarak değişir ve bu, AS'nin biyolojik aktivitelerini etkiler. Son yıllarda, literatürde ilaca (antibiyotik) dirençli patojenik bakteri miktarında aşırı miktarda artışa rastlanmaktadır. Antibiyotik direncinin artmasının ana nedenleri, antibiyotik kullanımının kötüye kullanılmasına bağlı olabilir. Bu durum antibiyotik direncinde ek bir birikmeyi önlemek için arı ürünleri gibi antibiyotik özellik taşıyan maddelerin diğer seçenekler olarak incelenmesinin önemini ortaya koymaktadır. Bingol AS'nin (BAS) kimyasal içeriği ve antimikrobiyal aktivitesi bugüne kadar araştırılmamıştır. Bu çalışma ile BAS’ın içeriği ve antimikrobiyal aktivitelerinin araştırılması amaçlanmıştır. Sonuçlar BAS’ın, antimikrobial ve antioksidan özelliklerine katkıda bulunan apigenin, quercetin, naringenin, gallik asit, kafeik asit gibi majör flavonoidler ve fenolikler içerdiğini göstermiştir. Aynı zamanda BAS’ın içeriğinde linoleik asit ve propionik asit gibi bazı orta ve kısa zincirli yağ asitlerinin varlığı da gösterilmiştir. BAS ayrıca eser elementlerin ve mineralin birçoğunu içermektedir. Kimyasal içeriğe ek olarak, BAS’ın antimikrobiyal aktivitesi de patojenlere karşı araştırılmış ve Salmonella typhimurium (8.64 mm), Escherichia coli (9.1 mm) ve Staphylococcus aureus'a (10.73 mm) karşı antimikrobiyal aktivite göstermiştir.
References
- Al-Abbadi, A.A. 2019. The Antimicrobial Potential of Royal Jelly against some Pathogenic Bacteria and Fungi. Jordan Journal of Biological Sciences, 12(4):445-451.
- Arshi, A., Jafari, M., Sadeghi, A., Gholami, M., Kabiri, H. and Abolhasani, M. 2019. Chrysin and its relation with gastric cancer. Journal of BioScience and Biotechnology, 8(1): 17-24.
- Asadi, N., Kheradmand, A., Gholami, M., Saidi, S.H. and Mirhadi, S.A. 2019. Effect of royal jelly on testicular antioxidant enzymes activity, MDA level and spermatogenesis in rat experimental Varicocele model. Tissue and Cell, 57: 70-77.
- Bărnuţiu, L.I., Mărghitaş, L.A., Dezmirean, D.S., Mihai, C.M. and Bobiş, O. 2011. Chemical composition and antimicrobial activity of Royal Jelly-REVIEW. Scientific Papers Animal Science and Biotechnologies, 44(2): 67-72.
- Basile, A., Giordano, S., López-Sáez, J.A. and Cobianchi, R.C. 1999. Antibacterial activity of pure flavonoids isolated from mosses. Phytochemistry, 52(8), 1479-1482.
- Caglayan, C., Kandemir, F.M., Yildirim, S., Kucukler, S. and Eser, G. 2019. Rutin protects mercuric chloride‐induced nephrotoxicity via targeting of aquaporin 1 level, oxidative stress, apoptosis and inflammation in rats. Journal of Trace Elements in Medicine and Biology, 54: 69-78.
- Chanwitheesuk, A., Teerawutgulrag, A., Kilburn, J.D. and Rakariyatham, N. 2007. Antimicrobial gallic acid from Caesalpinia mimosoides Lamk. Food Chemistry, 100(3): 1044-1048.
- Cornara, L., Biagi, M., Xiao, J. and Burlando, B. 2017. Therapeutic properties of bioactive compounds from different honeybee products. Frontiers in pharmacology, 8: 412-432.
- Coutinho, D., Karibasappa, S. N., & Mehta, D. S. 2018. Royal Jelly Antimicrobial Activity against Periodontopathic Bacteria. Journal of Interdisciplinary Dentistry, 8(1), 18-22.
- Danis, T.C.P., Madeira, V.M.C. and Almeida, M.L.M. 1994. Action of phenolic derivates (acetoaminophen, salycilate and 5-amino salycilate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Archives of Biochemistry and Biophysics, 315: 161-9.
- Demirel Sezer, E., Oktay, L.M., Karadadaş, E., Memmedov, H., Selvi Gunel, N. and Sözmen, E. 2019. Assessing Anticancer Potential of Blueberry Flavonoids, Quercetin, Kaempferol, and Gentisic Acid, Through Oxidative Stress and Apoptosis Parameters on HCT-116 Cells. Journal of medicinal food, 22(11): 1-9.
- Filipič, B., Gradišnik, L., Rihar, K., Šooš, E., Pereyra, A. and Potokar, J. 2015. The influence of royal jelly and human interferon-alpha (HuIFN-αN3) on proliferation, glutathione level and lipid peroxidation in human colorectal adenocarcinoma cells in vitro. Arhiv za higijenu rada i toksikologiju, 66(4): 0-0.
- Fratini, F., Cilia, G., Mancini, S. and Felicioli, A. 2016. Royal Jelly: An ancient remedy with remarkable antibacterial properties. Microbiological Research, 192: 130-141.
- Gu, H., Song, I.B., Han, H.J., Lee, N.Y., Cha, J.Y., Son, Y.K. and Kwon, J. 2018. Antioxidant Activity of Royal Jelly Hydrolysates Obtained by Enzymatic Treatment. Korean journal for food science of animal resources, 38(1): 135-142.
- Imran, M., Salehi, B., Sharifi-Rad, J., Aslam Gondal, T., Saeed, F., Imran, A., ... and Guerreiro, S.G. 2019. Kaempferol: A Key Emphasis to Its Anticancer Potential. Molecules, 24(12): 2277.
- Kaya, B., Darendelioğlu, E., Dervişoğlu, G., and 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.
- Khazaei, M. R., Makalani, F., Ghanbari, E., Fayzemahdavi, M. and Khazaei, M. 2018. An overview of effective herbal and antioxidant compounds on diabetes. Journal of Contemporary Medical Sciences, 4(3):126-133.
- 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. Oxidative medicine and cellular longevity, 1-29.
- López-Gutiérrez, N., del Mar Aguilera-Luiz, M., Romero-González, R., Vidal, J.L.M. and Frenich, A.G. 2014. Fast analysis of polyphenols in royal jelly products using automated TurboFlow™-liquid chromatography–Orbitrap high resolution mass spectrometry. Journal of Chromatography B, 973: 17-28.
Nabas, Z., Haddadin, M.S.Y., Haddadin, J. and Nazer, I.K. 2014. Chemical composition of royal jelly and effects of synbiotic with two different locally isolated probiotic strains on antioxidant activities. Polish Journal of Food and Nutrition Sciences, 64(3): 171-180.
- Nagai, T. and Inoue, R. 2004. Preparation and the functional properties of water extract and alkaline extract of royal jelly. Food chemistry, 84(2): 181-186.
- Nitiema, L. W., Savadogo, A., Simpore, J., Dianou, D. and Traore, A.S. 2012. In vitro antimicrobial activity of some phenolic compounds (coumarin and quercetin) against gastroenteritis bacterial strains. International Journal of Microbiology Research, 3(3): 183-187.
- Noori, A.L., Al Ghamdi, A., Ansari, M.J., Al-Attal, Y., Al-Mubarak, A. and Salom, K. 2013. Differences in composition of honey samples and their impact on the antimicrobial activities against drug multiresistant bacteria and pathogenic fungi. Archives of medical research, 44(4), 307-316.
- Nugent, R., Back, E. and Beith, A. 2010. The race against drug resistance. Washington (DC): Center for Global Development.
- Park, H.M., Cho, M.H., Cho, Y. and Kim, S.Y. 2012. Royal jelly increases collagen production in rat skin after ovariectomy. Journal of medicinal food, 15(6): 568-575.
- Park, H.G., Kim, B.Y., Park, M.J., Deng, Y., Choi, Y.S., Lee, K.S. and Jin, B.R. 2019. Antibacterial activity of major royal jelly proteins of the honeybee (Apis mellifera) royal jelly. Journal of Asia-Pacific Entomology.
- Pavel, C. I., Mărghitaş, L.A., Bobiş, O., Dezmirean, D.S., Şapcaliu, A., Radoi, I. and Mădaş, M.N. 2011. Biological activities of royal jelly-review. Scientific Papers Animal Science and Biotechnologies, 44(2): 108-118.
- Prieto, P., Pineda, M. and Aguilar, M. 1999. Spectrophotometric Quantitation of Antioxidant Capacity through the Formation of a Phosphomolybdenum Complex: Specific Application to the Determination of Vitamin E. Analytical Biochemistry, 269: 337-341.
- Ruch, R.J., Cheng, S.J. and Klaunig, J.E. 1989. Prevention of cytotoxicity and inhibition of intercellular communication by antioxidant catechins isolated from chinese green tea. Carcinogenesis, 10(6): 1003-1008.
- Šedivá, M., Laho, M., Kohútová, L., Mojžišová, A., Majtán, J. and Klaudiny, J. 2018. 10-HDA, A Major Fatty Acid of Royal Jelly, Exhibits pH Dependent Growth-Inhibitory Activity Against Different Strains of Paenibacillus larvae. Molecules, 23(12): 32-36.
- Stocker, A., Schramel, P., Kettrup, A. and Bengsch, E. 2005. Trace and mineral elements in royal jelly and homeostatic effects. Journal of Trace Elements in Medicine and Biology, 19:(2-3), 183-189.
- Taslimi, P., Kandemir, F.M., Demir, Y., İleritürk, M., Temel, Y., Caglayan, C. and Gulçin, İ. 2019. The antidiabetic and anticholinergic effects of chrysin on cyclophosphamide‐induced multiple organ toxicity in rats: Pharmacological evaluation of some metabolic enzyme activities. Journal of biochemical and molecular toxicology, e22313.
- Turk, E., Kandemir, F.M., Yildirim, S., Caglayan, C., Kucukler, S. and Kuzu, M. 2019. Protective effect of hesperidin on sodium arsenite-induced nephrotoxicity and hepatotoxicity in rats. Biological trace element research, 189(1): 95-108.
- Wang, B., Li, L., Fu, J., Yu, P., Gong, D., Zeng, C. And Zeng, Z. 2016. Effects of long‐chain and medium‐chain fatty acids on apoptosis and oxidative stress in human liver cells with steatosis. Journal of food science, 81(3): 794-800.
- WHO. World Health Organization. 2012. Antimicrobial Resistance. World Health Organization. Geneva.
- Yang, Y.C., Chou, W.M., Widowati, D.A., Lin, I.P. and Peng, C.C. 2018. 10-hydroxy-2-decenoic acid of royal jelly exhibits bactericide and anti-inflammatory activity in human colon cancer cells. BMC complementary and alternative medicine, 18(1):202-207.
- Yang, X., Li, Y., Wang, L., Li, L., Guo, L., Huang, F. and Zhao, H. 2019. Determination of 10‐Hydroxy‐2‐Decenoic Acid of Royal Jelly Using Near‐Infrared Spectroscopy Combined with Chemometrics. Journal of food science.