Antibacterial activity of Beehive Products
Subject Areas :
1 - Associate Professor, Department of Microbiology, Azadshahr branch, Islamic Azad University, Azadshahr, Iran
Keywords: Antibacterial activity, Bee products, Honey, Bee venom, Propolis, Royal jelly, Pollen,
Abstract :
Honeybees, also known as the "golden insect", belong to the genus Apis and the main species used for pollination of crops is Apis mellifera. Honeybees are one of the most amazing and economically useful insects. The products of this beneficial insect have been used for thousands of years in many cultures to treat various diseases, and their therapeutic properties have been recorded in many religious texts such as the Holy Quran. One of the most important biological activities of these products is their antibacterial activity. Each of the bee products, due to the presence of bioactive compounds, inhibits the growth of pathogenic bacterial strains. Due to the increasing spread of antibiotic resistance and unwanted side effects of chemical pharmaceutical compounds, the trend towards compounds of natural origin has increased to inhibit the growth of pathogenic microorganisms. Honey, venom, propolis, pollen, and royal jelly contain many bioactive compounds that make them effective against a variety of pathogenic bacterial species. Many studies have separately investigated the antibacterial activity of each of these products. The aim of the present study is to refer to the antibacterial activity of all honeybee products including honey, bee venom, propolis, pollen, and royal jelly in a focused study with emphasis on the mechanism of antibacterial activity of these products.
References:
Abd El-Wahed, A.A.; Khalifa, S.A.M.; Sheikh, B.Y.; Farag, M.A.; Saeed, A.; Larik, F.A. Chapter 13 Bee Venom Composition: From Chemistry to Biological Activity. In Studies in Natural Products Chemistry; Rahman, A.U., Ed.; Elsevier: Amsterdam, The Netherlands, 2019.
2. Abouda, Z., Zerdani, I., Kalalou, I., Faid, M., and Ahami, M. T., 2011. The antibacterial activity of Moroccan bee bread and bee-pollen (fresh and dried) against pathogenic bacteria. Research Journal of Microbiology. 6(4): 376. doi: 10.3923/jm.2011.376.384.
3. Adams, C. J., Manley-Harris, M., and Molan, P.C., 2009. The origin of methylglyoxal in New Zealand manuka (Leptospermum scoparium) honey. Carbohydrate research. 344(8): 1050-1053. doi: 10.1016/j.carres.2009.03.020.
4. Akbari, R., Hakemi Vala, M., Hashemi, A., Aghazadeh, H., Sabatier, J. M., and Pooshang Bagheri, K., 2018. Action mechanism of melittin-derived antimicrobial peptides, MDP1 and MDP2, de novo designed against multidrug resistant bacteria. Amino acids. 50: 1231-1243. doi: 10.1007/s00726-018-2596-5.
5. Alandejani, T., Marsan, J., Ferris, W., Slinger, R., and Chan, F., 2009. Effectiveness of honey on Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Otolaryngology—Head and Neck Surgery. 141(1): 114-118. doi: 10.1016/j.otohns.2009.01.005.
6. AL-Ani, I.; Zimmermann, S.; Reichling, J.; and Wink, M., 2015. Pharmacological synergism of bee venom and melittin with antibiotics and plant secondary metabolites against multi-drug resistant microbial pathogens. Phytomedicine. 22(2): 245–255. doi: 10.1016/j.phymed.2014.11.019.
7. Al-Ani, I., Zimmermann, S., Reichling, J., and Wink, M., 2018. Antimicrobial activities of European propolis collected from various geographic origins alone and in combination with antibiotics. Medicines. 5(1): 2. doi: 10.3390/medicines5010002.
8. Ali, B. M. M., Ghoname, N. F., Hodeib, A. A., and Elbadawy, M. A., 2015. Significance of topical propolis in the treatment of facial acne vulgaris. Egyptian Journal of Dermatology and Venerology. 35(1): 29-36. doi: 10.4103/1110-6530.162468.
9. Almeida, R. A. M. D. B., Olivo, T. E. T., Mendes, R. P., Barraviera, S. R. C. S., Souza, L. D. R., Martins, J. G., ... and Barraviera, B., 2011. Africanized honeybee stings: how to treat them. Revista da Sociedade Brasileira de Medicina Tropical. 44: 755-761. doi: 10.1590/s0037-86822011000600020.
10. Alvarez-Suarez, J. M., Gasparrini, M., Forbes-Hernández, T. Y., Mazzoni, L., and Giampieri, F., 2014. The composition and biological activity of honey: a focus on Manuka honey. Foods. 3(3): 420-432. doi: 10.3390/foods3030420.
11. Arteaga, V., Lamas, A., Regal, P., Vázquez, B., Miranda, J. M., Cepeda, A., and Franco, C. M. (2019). Antimicrobial activity of apitoxin from Apis mellifera in Salmonella enterica strains isolated from poultry and its effects on motility, biofilm formation and gene expression. Microbial pathogenesis. 137: 103771. doi: 10.1016/j.micpath.2019.103771.
12. Asthana, N., Yadav, S. P., and Ghosh, J. K. 2004. Dissection of antibacterial and toxic activity of melittin: a leucine zipper motif plays a crucial role in determining its hemolytic activity but not antibacterial activity. Journal of Biological Chemistry. 279(53): 55042-55050. doi: 10.1074/jbc.M408881200.
13. Bachanová, K., Klaudiny, J., Kopernický, J., and Šimúth, J. 2002. Identification of honeybee peptide active against Paenibacillus larvae larvae through bacterial growth-inhibition assay on polyacrylamide gel. Apidologie. 33(3): 259-269. doi:10.1051/apido:2002015.
14. Badet, C., and Quero, F. 2011. The in vitro effect of manuka honeys on growth and adherence of oral bacteria. Anaerobe. 17(1): 19-22. DOI: 10.1016/j.anaerobe.2010.12.007.
15. Bagheri, A., Koohsari, H., and Seyed Alangi, S. Z. 2016. Antibacterial and antioxidant activity of four types of honey with different floral origion. International Journal of Molecular and Clinical Microbiology. 6(2): 670-677.
16. Bagheri, A.; Koohsari, H.; Seyyed Alangi, S.Z., 2017. Antibacterial activity of monofloral and multifloral honeys with different floral origin in the Golestan province. Journal of Food Science and Technology. 62(14): 283-289.
17. Bang, L. M., Buntting, C., and Molan, P. 2003. The effect of dilution on the rate of hydrogen peroxide production in honey and its implications for wound healing. The Journal of Alternative and Complementary Medicine. 9(2): 267-273. doi: 10.1089/10755530360623383.
18. Bankova, V. S., de Castro, S. L., and Marcucci, M.C. 2000. Propolis: recent advances in chemistry and plant origin. Apidologie. 31(1): 3-15. DOI: 10.1051/apido:2000102.
19. Bastos, E. M. A., Simone, M., Jorge, D. M., Soares, A. E. E., and Spivak, M. 2008. In vitro study of the antimicrobial activity of Brazilian propolis against Paenibacillus larvae. Journal of Invertebrate Pathology. 97(3): 273-281. doi: 10.1016/j.jip.2007.10.007.
20. Bíliková, K., Mirgorodskaya, E., Bukovská, G., Gobom, J., Lehrach, H., and Šimúth, J. 2009. Towards functional proteomics of minority component of honeybee royal jelly: The effect of post‐translational modifications on the antimicrobial activity of apalbumin2. Proteomics. 9(8): 2131-2138. doi: 10.1002/pmic.200800705.
21. Bíliková, K., Wu, G., and Šimúth, J. 2001. Isolation of a peptide fraction from honeybee royal jelly as a potential antifoulbrood factor. Apidologie. 32(3): 275-283. DOI: 10.1051/apido:2001129.
22. Blaser, G., Santos, K., Bode, U., Vetter, H., and Simon, A. 2007. Effect of medical honey on wounds colonised or infected with MRSA. Journal of wound care. 16(8): 325-328. doi: 10.12968/jowc.2007.16.8.27851.
23. Boyanova, L., Ilieva, J., Gergova, G., Vladimirov, B., Nikolov, R., and Mitov, I. 2015. Honey and green/black tea consumption may reduce the risk of Helicobacter pylori infection. Diagnostic Microbiology and Infectious Disease. 82(1): 85-6. doi: 10.1016/j.diagmicrobio.2015.03.001.
24. Bogdanov, S. 2011. Royal jelly, bee brood: composition, health, medicine: a review. Lipids. 3(8): 8-19.
25. Bogdanov, S., and Henry, K. 2012. Propolis: Composition, Health, Medicine: A Review. Bee Product Science. 1–35.
26. Boukraâ, L., Abdellah, F., and Ait-Abderrahim, L. 2013. Antimicrobial properties of bee products and medicinal plants. Microbial pathogens and strategies for combating them: science, technology and education. URL: http://www. formatex. info/microbiology4/vol2. html (дата обращения: 20.05. 2017).
27. Bridi, R., Atala, E., Pizarro, P. N., and Montenegro, G. 2019. Honeybee pollen load: phenolic composition and antimicrobial activity and antioxidant capacity. Journal of natural products. 82(3): 559-565. DOI: 10.1021/acs.jnatprod.8b00945.
28. Brown, H. L., Metters, G., Hitchings, M. D., Wilkinson, T. S., Sousa, L., Cooper, J., ... and Jenkins, R. 2020. Antibacterial and antivirulence activity of Manuka Honey against genetically diverse Staphylococcus pseudintermedius strains. Applied and environmental microbiology. 86(20): e01768-20. doi: 10.1128/AEM.01768-20.
29. Brudzynski, K., Abubaker, K., and Miotto, D. 2012. Unraveling a mechanism of honey antibacterial action: Polyphenol/H2O2-induced oxidative effect on bacterial cell growth and on DNA degradation. Food chemistry. 133(2): 329-336. doi: 10.1016/j.foodchem.2012.01.035.
30. Brudzynski, K., and Lannigan, R. 2012. Mechanism of honey bacteriostatic action against MRSA and VRE involves hydroxyl radicals generated from honey’s hydrogen peroxide. Frontiers in microbiology. 3: 36. doi: 10.3389/fmicb.2012.00036.
31. Bucekova, M., Bugarova, V., Godocikova, J., and Majtan, J. 2020. Demanding new honey qualitative standard based on antibacterial activity. Foods. 9(9): 1263. doi: 10.3390/foods9091263.
32. Bucekova, M., and Majtan, J. 2016. The MRJP1 honey glycoprotein does not contribute to the overall antibacterial activity of natural honey. European Food Research and Technology. 242: 625-629. DOI: 10.1007/s00217-016-2665-5.
33. Buttstedt, A., Moritz, R. F., and Erler, S. 2013. More than royal food-Major royal jelly protein genes in sexuals and workers of the honeybee Apis mellifera. Frontiers in zoology. 10: 1-10. doi: 10.1186/1742-9994-10-72.
34. Buttstedt, A., Moritz, R. F., and Erler, S. 2014. Origin and function of the major royal jelly proteins of the honeybee (Apis mellifera) as members of the yellow gene family. Biological Reviews. 89(2): 255-269. doi: 10.1111/brv.12052.
35. Okamoto, I., Taniguchi, Y., Kunikata, T., Kohno, K., Iwaki, K., Ikeda, M., and Kurimoto, M. 2003. Major royal jelly protein 3 modulates immune responses in vitro and in vivo. Life sciences. 73(16): 2029-2045. doi: 10.1016/s0024-3205(03)00562-9.
36. Campos, M. G., Bogdanov, S., de Almeida-Muradian, L. B., Szczesna, T., Mancebo, Y., Frigerio, C., and Ferreira, F. 2008. Pollen composition and standardisation of analytical methods. Journal of Apicultural Research. 47(2): 154-161. doi: 10.3896/IBRA.1.47.2.12.
37. Campos, M. G. R., Frigerio, C., Lopes, J., and Bogdanov, S. 2010. What is the future of Bee Pollen. Journal of ApiProduct and ApiMedical Science, 2(4), 131-144. DOI: 10.3896/IBRA.4.02.4.01.
38. Choi, J. H., Jang, A. Y., Lin, S., Lim, S., Kim, D., Park, K., ... and Seo, H. S. 2015. Melittin, a honeybee venom derived antimicrobial peptide, may target methicillin resistant Staphylococcus aureus. Molecular medicine reports. 12(5): 6483-6490. doi: 10.3892/mmr.2015.4275.
39. Combarros-Fuertes, P., Fresno, J. M., Estevinho, M. M., Sousa-Pimenta, M., Tornadijo, M. E., and Estevinho, L. M. 2020a. Honey: another alternative in the fight against antibiotic-resistant bacteria? Antibiotics. 9(11): 774. doi: 10.3390/antibiotics9110774.
40. Combarros-Fuertes, P., M. Estevinho, L., Teixeira-Santos, R., G. Rodrigues, A., Pina-Vaz, C., Fresno, J. M., and Tornadijo, M. E. 2020b. Antibacterial action mechanisms of honey: Physiological Effects of Avocado, Chestnut, and Polyfloral Honey upon Staphylococcus aureus and Escherichia coli. Molecules. 25(5): 1252. doi: 10.3390/molecules25051252.
41. Cooper, R. A., Molan, P. C., and Harding, K. G. 2002. The sensitivity to honey of Gram‐positive cocci of clinical significance isolated from wounds. Journal of Applied microbiology. 93(5): 857-863. doi: 10.1046/j.1365-2672.2002.01761.x.
42. Cooper, R. A., Wigley, P., and Burton, N. F. 2000. Susceptibility of multiresistant strains of Burkholderia cepacia to honey. Letters in applied microbiology. 31(1): 20-24. doi: 10.1046/j.1472-765x.2000.00756.x.
43. Darwita, R. R., Finisha, A., Nur Wahyuni, H., Ghina, S., Muhammad, R., Satyanegara, A., ... and Adiatman, M. 2018. The effectiveness of propolis fluoride application in inhibiting dental caries activity in school children age 6-9 years old. International Journal of Applied Pharmaceutics. 9(1). doi: 10.22159/ijap.2017.v9s2.01.
44. Erkmen, O., and Özcan, M. M. 2008. Antimicrobial effects of Turkish propolis, pollen, and laurel on spoilage and pathogenic food-related microorganisms. Journal of medicinal food. 11(3): 587-592. doi: 10.1089/jmf.2007.0038.
45. Fadl, A. E.W. 2018. Antibacterial and antibiofilm effects of bee venom from (Apis mellifera) on multidrug-resistant bacteria (MDRB). Al-Azhar Journal of Pharmaceutical Sciences. 58(2): 60-80.
46. Fatrcová-Šramková, K., Nôžková, J., Kačániová, M., Máriássyová, M., Rovná, K., and Stričík, M. 2013. Antioxidant and antimicrobial properties of monofloral bee pollen. Journal of Environmental Science and Health, Part B. 48(2): 133-138. doi: 10.1080/03601234.2013.727664.
47. Fernandes Júnior, A., Balestrin, E. C., Betoni, J. E. C., Orsi, R. D. O., Cunha, M.D.L.R.D.S.D., and Montelli, A.C. 2005. Propolis: anti-Staphylococcus aureus activity and synergism with antimicrobial drugs. Memórias do Instituto Oswaldo Cruz. 100: 563-566. doi: 10.1590/s0074-02762005000500018.
48. Fitzgerald, K. T., and Flood, A.A. 2006. Hymenoptera stings. Clinical techniques in small animal practice. 21(4): 194-204. doi: 10.1053/j.ctsap.2006.10.002.
49. Fontana, R., Mendes, M. A., De Souza, B. M., Konno, K., César, L. M. M., Malaspina, O., and Palma, M. S. 2004. Jelleines: a family of antimicrobial peptides from the Royal Jelly of honeybees (Apis mellifera). Peptides. 25(6): 919-928. doi: 10.1016/j.peptides.2004.03.016.
50. Fratini, F., Cilia, G., Mancini, S., and Felicioli, A. 2016. Royal Jelly: An ancient remedy with remarkable antibacterial properties. Microbiological research. 192: 130-141. doi: 10.1016/j.micres.2016.06.007.
51. Fujiwara, S., Imai, J., Fujiwara, M., Yaeshima, T., Kawashima, T., and Kobayashi, K. 1990. A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. Journal of biological chemistry. 265(19): 11333-11337. doi: 5;265(19):11333-7.
52. Galeotti, F., Maccari, F., Fachini, A., and Volpi, N. 2018. Chemical composition and antioxidant activity of propolis prepared in different forms and in different solvents useful for finished products. Foods. 7(3): 41. doi: 10.3390/foods7030041.
53. García, M. C., Finola, M. S., and Marioli, J. M. 2010. Antibacterial activity of Royal Jelly against bacteria capable of infecting cutaneous wounds. Journal of ApiProduct and ApiMedical Science. 2(3): 93-99. Doi:10.3896/IBRA.4.02.3.02.
54. Garmani, M.; Koohsari, H.; Seyyed Alangi, S.Z., 2018. The antibactrial and antioxidant activity of several types of beepropolis collected from different geographic regions of Golestan province. Journal of Veterinary Microbiology. 14(2): 25-35.
55. Gebara, E. C. E., Pustiglioni, A. N., de Lima, L. A. P. A., and Mayer, M. P. A. 2003. Propolis extract as an adjuvant to periodontal treatment. Oral health and preventive dentistry. 1(1). PMID: 15643746.
56. Haji Mohammad, F., Koohsari, H., and Ghaboos, S. H. 2022. Antibacterial and antioxidant activity of royal jelly collected from geographical regions with different climates in the north of Iran. Bulgarian Journal of Veterinary Medicine. 25(3): 397-410. doi: 10.15547/bjvm.2020-0133.
57. Hanes, J., and Šimuth, J. 1992. Identification and partial characterization of the major royal jelly protein of the honey bee (Apis mellifera L.). Journal of Apicultural Research. 31(1): 22-26. doi:10.1080/00218839.1992.11101256.
58. Han, S. M., Lee, K. G., and Pak, S.C. 2013. Effects of cosmetics containing purified honeybee (Apis mellifera L.) venom on acne vulgaris. Journal of integrative medicine. 11(5): 320-326. doi: 10.3736/jintegrmed2013043.
59. Han, S., Yeo, J., Baek, H., Lin, S. M., Meyer, S., and Molan, P. 2009. Postantibiotic effect of purified melittin from honeybee (Apis mellifera) venom against Escherichia coli and Staphylococcus aureus. Journal of Asian natural products research. 11(9): 796-804. doi: 10.1080/10286020903164277.
60. Header, E., Hashish, A. E. M., ElSawy, N., Al-Kushi, A., and El-Boshy, M. 2016. Gastroprotective effects of dietary honey against acetylsalicylate induced experimental gastric ulcer in albino rats. Life Science Journal. 13(1): 42-47.
61. Hegazi, A. G., El-Feel, M. A., Abdel-Rahman, E., and Al-Fattah, A. 2015. Antibacterial activity of bee venom collected from Apis mellifera carniolan pure and hybrid races by two collection methods. International Journal of Current Microbiology and Applied Sciences. 4(4): 141-9.
62. Hermanns, R., Mateescu, C., Thrasyvoulou, A., Tananaki, C., Wagener, F. A., and Cremers, N.A. 2020. Defining the standards for medical grade honey. Journal of apicultural research. 59(2): 125-135. doi: 10.1080/00218839.2019.1693713.
63. Hizomi Shirejini, S., Koohsari, H., and Seyed Alangi, S. Z. 2018. Antibacterial activity and physico-chemical analysis of several types of honey with different floral origins in the Golestan province. Iranian Food Science and Technology Research Journal. 14(2): 273-282. DOI: 10.22067/ifstrj.v0i0.60915.
64. Inui, S., Hatano, A., Yoshino, M., Hosoya, T., Shimamura, Y., Masuda, S., ... and Kumazawa, S. 2014. Identification of the phenolic compounds contributing to antibacterial activity in ethanol extracts of Brazilian red propolis. Natural product research. 28(16): 1293-1296. doi: 10.1080/14786419.2014.898146.
65. Issam, A. A., Zimmermann, S., Reichling, J., and Wink, M. 2015. Pharmacological synergism of bee venom and melittin with antibiotics and plant secondary metabolites against multi-drug resistant microbial pathogens. Phytomedicine. 22(2): 245-255. doi: 10.1016/j.phymed.2014.11.019.
66. Jamasbi, E., Batinovic, S., Sharples, R. A., Sani, M. A., Robins-Browne, R. M., Wade, J. D., ... and Hossain, M.A. 2014. Melittin peptides exhibit different activity on different cells and model membranes. Amino acids. 46: 2759-2766. doi: 10.1007/s00726-014-1833-9.
67. Jenkins, R. and Cooper, R. 2012. Improving antibiotic activity against wound pathogens with manuka honey in vitro. PLoS ONE. 2012, 7: e45600. doi: 10.1371/journal.pone.0045600.
68. Kacaniova, M.; Vukovic´, N.; Chlebo, R.; Hašcík, P.; Rovná, K.; Cubon, J., ... and Pasternakiewicz, A. 2012. The antimicrobial activity of honey, bee pollen loads and beeswax from Slovakia. Archives of Biological Sciences. 64: 927–934. doi: 10.2298/ABS1203927K.
69. Kačániová, M., Vatl'ák, A., Vuković, N., Petrová, J., Brindza, J., Nôžková, J., and Fatrcová-Šrámková, K. 2014. Antimicrobial activity of bee collected pollen against clostridia. Animal Science and Biotechnologies, 47(2): 362-365.
70. Karadal, F., Onmaz, N. E., Abay, S., Yildirim, Y., Al, S., Tatyuz, I., and Akcay, A. 2018. A study of antibacterial and antioxidant activities of bee products: Propolis, pollen and honey samples. Ethiopian Journal of Health Development. 32(2).
71. Kaškonienė, V., Adaškevičiūtė, V., Kaškonas, P., Mickienė, R., and Maruška, A. 2020. Antimicrobial and antioxidant activities of natural and fermented bee pollen. Food bioscience. 34 100532. doi: 10.1016/j.fbio.2020.100532.
72. Kharsany, K., Viljoen, A., Leonard, C., and Van Vuuren, S. 2019. The new buzz: Investigating the antimicrobial interactions between bioactive compounds found in South African propolis. Journal of ethnopharmacology. 238: 111867. doi: 10.1016/j.jep.2019.111867.
73. Khider, M., Elbanna, K., Mahmoud, A., and Owayss, A.A. 2013. Egyptian honeybee pollen as antimicrobial, antioxidant agents, and dietary food supplements. Food science and biotechnology. 22: 1-9. doi: 10.1007/s10068-013-0238-y.
74. Khosla, A., Gupta, S. J., Jain, A., Shetty, D. C., and Sharma, N. 2020. Evaluation and comparison of the antimicrobial activity of royal jelly–A holistic healer against periodontopathic bacteria: An: in vitro: study. Journal of Indian Society of Periodontology. 24(3): 221-226. doi: 10.4103/jisp.jisp_486_19.
75. Kilic, A., Baysallar, M., Besırbellıoglu, B., Salıh, B., Sorkun, K. A. D. R. İ. Y. E., and Tanyuksel, M. 2005. In vitro antimicrobial activity of propolis against methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus faecium. 113-117.
76. Kim, H., Park, S. Y., and Lee, G. 2019. Potential therapeutic applications of bee venom on skin disease and its mechanisms: A literature review. Toxins. 11(7): 374. doi: 10.3390/toxins11070374.
77. Koru, O., Toksoy, F., Acikel, C. H., Tunca, Y. M., Baysallar, M., Guclu, A. U., ... and Salih, B. 2007. In vitro antimicrobial activity of propolis samples from different geographical origins against certain oral pathogens. Anaerobe. 13(3-4): 140-145. doi: 10.1016/j.anaerobe.2007.02.001.
78. Kroyer, G., and Hegedus, N. 2001. Evaluation of bioactive properties of pollen extracts as functional dietary food supplement. Innovative Food Science and Emerging Technologies. 2(3): 171-174. doi: 10.1016/S1466-8564(01)00039-X.
79. Kumar, P., Sindhu, R. K., Narayan, S., and Singh, I. 2010. Honey collected from different floras of Chandigarh Tricity: A comparative study involving physicochemical parameters and biochemical activities. Journal of dietary supplements. 7(4): 303-313. doi: 10.3109/19390211.2010.508034.
80. Kuropatnicki, A. K., Szliszka, E., and Krol, W. 2013. Historical aspects of propolis research in modern times. Evidence‐Based Complementary and Alternative Medicine, 2013(1), 964149. doi: 10.1155/2013/964149.
81. Kwakman, P. H., Velde, A. A. T., de Boer, L., Speijer, D., Christina Vandenbroucke‐Grauls, M. J., and Zaat, S.A. 2010. How honey kills bacteria. The FASEB Journal. 24(7): 2576-2582. doi: 10.1096/fj.09-150789.
82. Melliou, E., and Chinou, I. 2005. Chemistry and bioactivity of royal jelly from Greece. Journal of agricultural and food chemistry. 53(23): 8987-8992. doi: 10.1021/jf051550p.
83. Mokaya, H. O., Bargul, J. L., Irungu, J. W., and Lattorff, H. M.G. 2020. Bioactive constituents, in vitro radical scavenging and antibacterial activities of selected Apis mellifera honey from Kenya. International journal of food science and technology. 55(3): 1246-1254. doi: 10.1111/ijfs.14403.
84. Morais, M., Moreira, L., Feás, X., and Estevinho, L.M. 2011. Honeybee-collected pollen from five Portuguese Natural Parks: Palynological origin, phenolic content, antioxidant properties and antimicrobial activity. Food and Chemical Toxicology. 49(5): 1096-1101. doi: 10.1016/j.fct.2011.01.020.
85. Leandro, L. F., Mendes, C. A., Casemiro, L. A., Vinholis, A. H., Cunha, W. R., Almeida, R. D., and Martins, C.H. 2015. Antimicrobial activity of apitoxin, melittin and phospholipase A2 of honey bee (Apis mellifera) venom against oral pathogens. Anais da Academia Brasileira de Ciências. 87(01): 147-155. doi: 10.1590/0001-3765201520130511.
86. Miguel, M. G., Nunes, S., Dandlen, S. A., Cavaco, A. M., and Antunes, M.D. 2010. Phenols and antioxidant activity of hydro-alcoholic extracts of propolis from Algarve, South of Portugal. Food and Chemical Toxicology. 48(12): 3418-3423. doi: 10.1016/j.fct.2010.09.014.
87. Molan, P. C., and Allen, K.L. 1996. The effect of gamma‐irradiation on the antibacterial activity of honey. Journal of pharmacy and pharmacology. 48(11): 1206-1209. doi: 10.1111/j.2042-7158.1996.tb03922.x.
88. Molan, P.C. 1992. The antibacterial activity of honey: 2 Variation in the potency of the antibacterial activity. Bee World. 73(2): 59-76. doi.org/10.1080/0005772X.1992.11099118.
89. Moniruzzaman, M., Khalil, M. I., Sulaiman, S. A., and Gan, S. H. 2013. Physicochemical and antioxidant properties of Malaysian honeys produced by Apis cerana, Apis dorsata and Apis mellifera. BMC Complementary and Alternative Medicine. 13: 1-12. doi: 10.1186/1472-6882-13-43.
90. Nader, R.A.; Mackieh, R.; Wehbe, R.; El Obeid, D.; Sabatier, J.M.; Fajloun, Z. 2021. Beehive Products as Antibacterial Agents: A Review. Antibiotics, 10: 717. https://doi.org/10.3390/antibiotics10060717.
91. Okińczyc, P., Paluch, E., Franiczek, R., Widelski, J., Wojtanowski, K. K., Mroczek, T., ... and Sroka, Z. (2020). Antimicrobial activity of Apis mellifera L. and Trigona sp. propolis from Nepal and its phytochemical analysis. Biomedicine and Pharmacotherapy. 129: 110435. doi: 10.1016/j.biopha.2020.110435.
92. Orsi, R. D. O., Fernandes, A., Bankova, V., and Sforcin, J. M. 2012. The effects of Brazilian and Bulgarian propolis in vitro against Salmonella Typhi and their synergism with antibiotics acting on the ribosome. Natural product research. 26(5): 430-437. doi: 10.1080/14786419.2010.498776.
93. Pucca, M. B., Cerni, F. A., Oliveira, I. S., Jenkins, T. P., Argemí, L., Sørensen, C. V., ... and Laustsen, A.H. 2019. Bee updated: current knowledge on bee venom and bee envenoming therapy. Frontiers in immunology. 10: 2090. doi: 10.3389/fimmu.2019.02090.
94. Ratanavalachai, T., and Wongchai, V. 2002. Antibacterial activity of intact roval jelly, its lipid extract and its defatted extract. Science and Technology Asia. 7: 5-12.
95. Rosmilah, M., Shahnaz, M., Patel, G., Lock, J., Rahman, D., Masita, A., and Noormalin, A. 2008. Characterization of major allergens of royal jelly Apis mellifera. Tropical Biomedicine. 25: 243–251. Doi: ;25(3):243-51.
96. 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): 3236. doi.org/10.3390/molecules23123236.
97. Seibert, J. B., Bautista-Silva, J. P., Amparo, T. R., Petit, A., Pervier, P., dos Santos Almeida, J. C., ... and Dos Santos, O.D.H. 2019. Development of propolis nanoemulsion with antioxidant and antimicrobial activity for use as a potential natural preservative. Food chemistry. 287: 61-67. doi: 10.1016/j.foodchem.2019.02.078.
98. Seidel, V., Peyfoon, E., Watson, D. G., and Fearnley, J. 2008. Comparative study of the antibacterial activity of propolis from different geographical and climatic zones. Phytotherapy research. 22(9): 1256-1263. doi: 10.1002/ptr.2480.
99. Shabbir, A., Rashid, M., and Tipu, H.N. 2016. Propolis, a hope for the future in treating resistant periodontal pathogens. Cureus. 8(7): e682. doi: 10.7759/cureus.682.
100. Shakiba, E., Koohsari, H., and Mahmoodjanloo, M.A. 2018. Antibacterial Activity of Honey Bee Products Collected from Three Different Climate in Golestan Province in Northern Iran. International Journal of Molecular and Clinical Microbiology. 8(2): 1062-1073.
101. Shen LiRong, S. L., Liu DanDan, L. D., Li MeiLu, L. M., Jin Feng, J. F., Din MeiHui, D. M., Parnell, L. D., and Lai, C.Q. 2012. Mechanism of action of recombinant Acc-royalisin from royal jelly of Asian honeybee against Gram-positive bacteria. PLoS ONE. 7: e47194. doi: 10.1371/journal.pone.0047194.
102. Šimunovic, K.; Abramovi, H.; Lilek, N.; Angelova, M.; Podržaj, L.; Smole Možina, S.S. 2019. Microbiological quality, antioxidantive and antimicrobial properties of Slovenian bee pollen. Agrofor, 4(1). 4: 82–92. doi: 10.7251/AGRENG1901082S.
103. Sowa, P., Grabek‐Lejko, D., Wesołowska, M., Swacha, S., and Dżugan, M. 2017. Hydrogen peroxide‐dependent antibacterial action of Melilotus albus honey. Letters in applied microbiology. 65(1): 82-89. doi: 10.1111/lam.12749.
104. Szweda, P. 2017. Antimicrobial Activity of Honey. Honey analysis. Croatia, Intech, Open. 17: 216-228. doi: 10.5772/67117.
105. Taha, E. K. A., Al-Kahtani, S., and Taha, R. 2019. Protein content and amino acids composition of bee-pollens from major floral sources in Al-Ahsa, eastern Saudi Arabia. Saudi Journal of Biological Sciences. 26(2): 232-237. doi: 10.1016/j.sjbs.2017.06.003.
106. Veiga, R. S., De Mendonça, S., Mendes, P. B., Paulino, N., Mimica, M. J., Lagareiro Netto, A. A., ... and Marcucci, M. C. 2017. Artepillin C and phenolic compounds responsible for antimicrobial and antioxidant activity of green propolis and Baccharis dracunculifolia DC. Journal of Applied Microbiology. 122(4): 911-920. doi: 10.1111/jam.13400.
107. Velásquez, P., Rodriguez, K., Retamal, M., Giordano Villatoro, A., Valenzuela Roediger, L. M., and Montenegro Rizzardini, G. 2017. Relation between composition, antioxidant and antibacterial activities and botanical origin of multi-floral bee pollen. Journal of Applied Botany and Food Quality. 90: 306–314.
108. Veloz, J. J., Alvear, M., and Salazar, L. A. 2019. Antimicrobial and antibiofilm activity against Streptococcus mutans of individual and mixtures of the main polyphenolic compounds found in Chilean propolis. BioMed research international. 2019(1): 7602343. doi: 10.1155/2019/7602343.
109. Wang, L., Zhao, X., Zhu, C., Zhao, Y., Liu, S., Xia, X., ... and Hu, J. 2020. The antimicrobial peptide MPX kills Actinobacillus pleuropneumoniae and reduces its pathogenicity in mice. Veterinary microbiology. 243: 108634. doi: 10.1016/j.vetmic.2020.108634.
110. Wehbe, R., Frangieh, J., Rima, M., El Obeid, D., Sabatier, J. M., and Fajloun, Z. 2019. Bee venom: Overview of main compounds and bioactivities for therapeutic interests. Molecules. 24(16): 2997. doi: 10.3390/molecules24162997.
111. Wilkinson, J. M., and Cavanagh, H. M. 2005. Antibacterial activity of 13 honeys against Escherichia coli and Pseudomonas aeruginosa. Journal of medicinal food. 8(1): 100-103. doi: 10.1089/jmf.2005.8.100.
112. Wojtyczka, R. D., Dziedzic, A., Idzik, D., Kępa, M., Kubina, R., Kabała-Dzik, A., ... and Wąsik, T. J. 2013. Susceptibility of Staphylococcus aureus clinical isolates to propolis extract alone or in combination with antimicrobial drugs. Molecules. 18(8): 9623-9640. doi: 10.3390/molecules18089623.
113. Wu, X., Singh, A. K., Wu, X., Lyu, Y., Bhunia, A. K., and Narsimhan, G. 2016. Characterization of antimicrobial activity against Listeria and cytotoxicity of native melittin and its mutant variants. Colloids and Surfaces B: Biointerfaces. 143: 194-205. doi: 10.1016/j.colsurfb.2016.03.037.
114. Yacoub, T., Rima, M., Karam, M., Sabatier, J. M., and Fajloun, Z. 2020. Antimicrobials from venomous animals: An overview. Molecules. 25(10): 2402. doi: 10.3390/molecules25102402.
115. Yazdani, Amin; Koohsari, Hadi; Sadegh Shesh Poli, Maryam. Antibacterial Activity of Honey and Bee Pollen Collected from Bee Hives from Three Climatic Regions of Golestan Province Against some Clinical Isolates with High Antibiotic Resistance. Research and Innovation in Food Science and Technology. 2024. doi: 10.22101/jrifst.2024.415662.1514.
116. Yoshimasu, Y., Ikeda, T., Sakai, N., Yagi, A., Hirayama, S., Morinaga, Y., ... and Nakao, R. 2018. Rapid bactericidal action of propolis against Porphyromonas gingivalis. Journal of dental research. 97(8): 928-936. doi: 10.1177/0022034518758034.
117. Yousaf, I., Ishaq, I., Hussain, M. B., Inaam, S., Saleem, S., and Qamar, M. U. 2019. Antibacterial activity of Pakistani Beri honey compared with silver sulfadiazine on infected wounds: a clinical trial. Journal of Wound Care. 28(5): 291-296. doi: 10.12968/jowc.2019.28.5.291.
Abd El-Wahed, A.A.; Khalifa, S.A.M.; Sheikh, B.Y.; Farag, M.A.; Saeed, A.; Larik, F.A. Chapter 13 Bee Venom Composition: From Chemistry to Biological Activity. In Studies in Natural Products Chemistry; Rahman, A.U., Ed.; Elsevier: Amsterdam, The Netherlands, 2019.
2. Abouda, Z., Zerdani, I., Kalalou, I., Faid, M., and Ahami, M. T., 2011. The antibacterial activity of Moroccan bee bread and bee-pollen (fresh and dried) against pathogenic bacteria. Research Journal of Microbiology. 6(4): 376. doi: 10.3923/jm.2011.376.384.
3. Adams, C. J., Manley-Harris, M., and Molan, P.C., 2009. The origin of methylglyoxal in New Zealand manuka (Leptospermum scoparium) honey. Carbohydrate research. 344(8): 1050-1053. doi: 10.1016/j.carres.2009.03.020.
4. Akbari, R., Hakemi Vala, M., Hashemi, A., Aghazadeh, H., Sabatier, J. M., and Pooshang Bagheri, K., 2018. Action mechanism of melittin-derived antimicrobial peptides, MDP1 and MDP2, de novo designed against multidrug resistant bacteria. Amino acids. 50: 1231-1243. doi: 10.1007/s00726-018-2596-5.
5. Alandejani, T., Marsan, J., Ferris, W., Slinger, R., and Chan, F., 2009. Effectiveness of honey on Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Otolaryngology—Head and Neck Surgery. 141(1): 114-118. doi: 10.1016/j.otohns.2009.01.005.
6. AL-Ani, I.; Zimmermann, S.; Reichling, J.; and Wink, M., 2015. Pharmacological synergism of bee venom and melittin with antibiotics and plant secondary metabolites against multi-drug resistant microbial pathogens. Phytomedicine. 22(2): 245–255. doi: 10.1016/j.phymed.2014.11.019.
7. Al-Ani, I., Zimmermann, S., Reichling, J., and Wink, M., 2018. Antimicrobial activities of European propolis collected from various geographic origins alone and in combination with antibiotics. Medicines. 5(1): 2. doi: 10.3390/medicines5010002.
8. Ali, B. M. M., Ghoname, N. F., Hodeib, A. A., and Elbadawy, M. A., 2015. Significance of topical propolis in the treatment of facial acne vulgaris. Egyptian Journal of Dermatology and Venerology. 35(1): 29-36. doi: 10.4103/1110-6530.162468.
9. Almeida, R. A. M. D. B., Olivo, T. E. T., Mendes, R. P., Barraviera, S. R. C. S., Souza, L. D. R., Martins, J. G., ... and Barraviera, B., 2011. Africanized honeybee stings: how to treat them. Revista da Sociedade Brasileira de Medicina Tropical. 44: 755-761. doi: 10.1590/s0037-86822011000600020.
10. Alvarez-Suarez, J. M., Gasparrini, M., Forbes-Hernández, T. Y., Mazzoni, L., and Giampieri, F., 2014. The composition and biological activity of honey: a focus on Manuka honey. Foods. 3(3): 420-432. doi: 10.3390/foods3030420.
11. Arteaga, V., Lamas, A., Regal, P., Vázquez, B., Miranda, J. M., Cepeda, A., and Franco, C. M. (2019). Antimicrobial activity of apitoxin from Apis mellifera in Salmonella enterica strains isolated from poultry and its effects on motility, biofilm formation and gene expression. Microbial pathogenesis. 137: 103771. doi: 10.1016/j.micpath.2019.103771.
12. Asthana, N., Yadav, S. P., and Ghosh, J. K. 2004. Dissection of antibacterial and toxic activity of melittin: a leucine zipper motif plays a crucial role in determining its hemolytic activity but not antibacterial activity. Journal of Biological Chemistry. 279(53): 55042-55050. doi: 10.1074/jbc.M408881200.
13. Bachanová, K., Klaudiny, J., Kopernický, J., and Šimúth, J. 2002. Identification of honeybee peptide active against Paenibacillus larvae larvae through bacterial growth-inhibition assay on polyacrylamide gel. Apidologie. 33(3): 259-269. doi:10.1051/apido:2002015.
14. Badet, C., and Quero, F. 2011. The in vitro effect of manuka honeys on growth and adherence of oral bacteria. Anaerobe. 17(1): 19-22. DOI: 10.1016/j.anaerobe.2010.12.007.
15. Bagheri, A., Koohsari, H., and Seyed Alangi, S. Z. 2016. Antibacterial and antioxidant activity of four types of honey with different floral origion. International Journal of Molecular and Clinical Microbiology. 6(2): 670-677.
16. Bagheri, A.; Koohsari, H.; Seyyed Alangi, S.Z., 2017. Antibacterial activity of monofloral and multifloral honeys with different floral origin in the Golestan province. Journal of Food Science and Technology. 62(14): 283-289.
17. Bang, L. M., Buntting, C., and Molan, P. 2003. The effect of dilution on the rate of hydrogen peroxide production in honey and its implications for wound healing. The Journal of Alternative and Complementary Medicine. 9(2): 267-273. doi: 10.1089/10755530360623383.
18. Bankova, V. S., de Castro, S. L., and Marcucci, M.C. 2000. Propolis: recent advances in chemistry and plant origin. Apidologie. 31(1): 3-15. DOI: 10.1051/apido:2000102.
19. Bastos, E. M. A., Simone, M., Jorge, D. M., Soares, A. E. E., and Spivak, M. 2008. In vitro study of the antimicrobial activity of Brazilian propolis against Paenibacillus larvae. Journal of Invertebrate Pathology. 97(3): 273-281. doi: 10.1016/j.jip.2007.10.007.
20. Bíliková, K., Mirgorodskaya, E., Bukovská, G., Gobom, J., Lehrach, H., and Šimúth, J. 2009. Towards functional proteomics of minority component of honeybee royal jelly: The effect of post‐translational modifications on the antimicrobial activity of apalbumin2. Proteomics. 9(8): 2131-2138. doi: 10.1002/pmic.200800705.
21. Bíliková, K., Wu, G., and Šimúth, J. 2001. Isolation of a peptide fraction from honeybee royal jelly as a potential antifoulbrood factor. Apidologie. 32(3): 275-283. DOI: 10.1051/apido:2001129.
22. Blaser, G., Santos, K., Bode, U., Vetter, H., and Simon, A. 2007. Effect of medical honey on wounds colonised or infected with MRSA. Journal of wound care. 16(8): 325-328. doi: 10.12968/jowc.2007.16.8.27851.
23. Boyanova, L., Ilieva, J., Gergova, G., Vladimirov, B., Nikolov, R., and Mitov, I. 2015. Honey and green/black tea consumption may reduce the risk of Helicobacter pylori infection. Diagnostic Microbiology and Infectious Disease. 82(1): 85-6. doi: 10.1016/j.diagmicrobio.2015.03.001.
24. Bogdanov, S. 2011. Royal jelly, bee brood: composition, health, medicine: a review. Lipids. 3(8): 8-19.
25. Bogdanov, S., and Henry, K. 2012. Propolis: Composition, Health, Medicine: A Review. Bee Product Science. 1–35.
26. Boukraâ, L., Abdellah, F., and Ait-Abderrahim, L. 2013. Antimicrobial properties of bee products and medicinal plants. Microbial pathogens and strategies for combating them: science, technology and education. URL: http://www. formatex. info/microbiology4/vol2. html (дата обращения: 20.05. 2017).
27. Bridi, R., Atala, E., Pizarro, P. N., and Montenegro, G. 2019. Honeybee pollen load: phenolic composition and antimicrobial activity and antioxidant capacity. Journal of natural products. 82(3): 559-565. DOI: 10.1021/acs.jnatprod.8b00945.
28. Brown, H. L., Metters, G., Hitchings, M. D., Wilkinson, T. S., Sousa, L., Cooper, J., ... and Jenkins, R. 2020. Antibacterial and antivirulence activity of Manuka Honey against genetically diverse Staphylococcus pseudintermedius strains. Applied and environmental microbiology. 86(20): e01768-20. doi: 10.1128/AEM.01768-20.
29. Brudzynski, K., Abubaker, K., and Miotto, D. 2012. Unraveling a mechanism of honey antibacterial action: Polyphenol/H2O2-induced oxidative effect on bacterial cell growth and on DNA degradation. Food chemistry. 133(2): 329-336. doi: 10.1016/j.foodchem.2012.01.035.
30. Brudzynski, K., and Lannigan, R. 2012. Mechanism of honey bacteriostatic action against MRSA and VRE involves hydroxyl radicals generated from honey’s hydrogen peroxide. Frontiers in microbiology. 3: 36. doi: 10.3389/fmicb.2012.00036.
31. Bucekova, M., Bugarova, V., Godocikova, J., and Majtan, J. 2020. Demanding new honey qualitative standard based on antibacterial activity. Foods. 9(9): 1263. doi: 10.3390/foods9091263.
32. Bucekova, M., and Majtan, J. 2016. The MRJP1 honey glycoprotein does not contribute to the overall antibacterial activity of natural honey. European Food Research and Technology. 242: 625-629. DOI: 10.1007/s00217-016-2665-5.
33. Buttstedt, A., Moritz, R. F., and Erler, S. 2013. More than royal food-Major royal jelly protein genes in sexuals and workers of the honeybee Apis mellifera. Frontiers in zoology. 10: 1-10. doi: 10.1186/1742-9994-10-72.
34. Buttstedt, A., Moritz, R. F., and Erler, S. 2014. Origin and function of the major royal jelly proteins of the honeybee (Apis mellifera) as members of the yellow gene family. Biological Reviews. 89(2): 255-269. doi: 10.1111/brv.12052.
35. Okamoto, I., Taniguchi, Y., Kunikata, T., Kohno, K., Iwaki, K., Ikeda, M., and Kurimoto, M. 2003. Major royal jelly protein 3 modulates immune responses in vitro and in vivo. Life sciences. 73(16): 2029-2045. doi: 10.1016/s0024-3205(03)00562-9.
36. Campos, M. G., Bogdanov, S., de Almeida-Muradian, L. B., Szczesna, T., Mancebo, Y., Frigerio, C., and Ferreira, F. 2008. Pollen composition and standardisation of analytical methods. Journal of Apicultural Research. 47(2): 154-161. doi: 10.3896/IBRA.1.47.2.12.
37. Campos, M. G. R., Frigerio, C., Lopes, J., and Bogdanov, S. 2010. What is the future of Bee Pollen. Journal of ApiProduct and ApiMedical Science, 2(4), 131-144. DOI: 10.3896/IBRA.4.02.4.01.
38. Choi, J. H., Jang, A. Y., Lin, S., Lim, S., Kim, D., Park, K., ... and Seo, H. S. 2015. Melittin, a honeybee venom derived antimicrobial peptide, may target methicillin resistant Staphylococcus aureus. Molecular medicine reports. 12(5): 6483-6490. doi: 10.3892/mmr.2015.4275.
39. Combarros-Fuertes, P., Fresno, J. M., Estevinho, M. M., Sousa-Pimenta, M., Tornadijo, M. E., and Estevinho, L. M. 2020a. Honey: another alternative in the fight against antibiotic-resistant bacteria? Antibiotics. 9(11): 774. doi: 10.3390/antibiotics9110774.
40. Combarros-Fuertes, P., M. Estevinho, L., Teixeira-Santos, R., G. Rodrigues, A., Pina-Vaz, C., Fresno, J. M., and Tornadijo, M. E. 2020b. Antibacterial action mechanisms of honey: Physiological Effects of Avocado, Chestnut, and Polyfloral Honey upon Staphylococcus aureus and Escherichia coli. Molecules. 25(5): 1252. doi: 10.3390/molecules25051252.
41. Cooper, R. A., Molan, P. C., and Harding, K. G. 2002. The sensitivity to honey of Gram‐positive cocci of clinical significance isolated from wounds. Journal of Applied microbiology. 93(5): 857-863. doi: 10.1046/j.1365-2672.2002.01761.x.
42. Cooper, R. A., Wigley, P., and Burton, N. F. 2000. Susceptibility of multiresistant strains of Burkholderia cepacia to honey. Letters in applied microbiology. 31(1): 20-24. doi: 10.1046/j.1472-765x.2000.00756.x.
43. Darwita, R. R., Finisha, A., Nur Wahyuni, H., Ghina, S., Muhammad, R., Satyanegara, A., ... and Adiatman, M. 2018. The effectiveness of propolis fluoride application in inhibiting dental caries activity in school children age 6-9 years old. International Journal of Applied Pharmaceutics. 9(1). doi: 10.22159/ijap.2017.v9s2.01.
44. Erkmen, O., and Özcan, M. M. 2008. Antimicrobial effects of Turkish propolis, pollen, and laurel on spoilage and pathogenic food-related microorganisms. Journal of medicinal food. 11(3): 587-592. doi: 10.1089/jmf.2007.0038.
45. Fadl, A. E.W. 2018. Antibacterial and antibiofilm effects of bee venom from (Apis mellifera) on multidrug-resistant bacteria (MDRB). Al-Azhar Journal of Pharmaceutical Sciences. 58(2): 60-80.
46. Fatrcová-Šramková, K., Nôžková, J., Kačániová, M., Máriássyová, M., Rovná, K., and Stričík, M. 2013. Antioxidant and antimicrobial properties of monofloral bee pollen. Journal of Environmental Science and Health, Part B. 48(2): 133-138. doi: 10.1080/03601234.2013.727664.
47. Fernandes Júnior, A., Balestrin, E. C., Betoni, J. E. C., Orsi, R. D. O., Cunha, M.D.L.R.D.S.D., and Montelli, A.C. 2005. Propolis: anti-Staphylococcus aureus activity and synergism with antimicrobial drugs. Memórias do Instituto Oswaldo Cruz. 100: 563-566. doi: 10.1590/s0074-02762005000500018.
48. Fitzgerald, K. T., and Flood, A.A. 2006. Hymenoptera stings. Clinical techniques in small animal practice. 21(4): 194-204. doi: 10.1053/j.ctsap.2006.10.002.
49. Fontana, R., Mendes, M. A., De Souza, B. M., Konno, K., César, L. M. M., Malaspina, O., and Palma, M. S. 2004. Jelleines: a family of antimicrobial peptides from the Royal Jelly of honeybees (Apis mellifera). Peptides. 25(6): 919-928. doi: 10.1016/j.peptides.2004.03.016.
50. Fratini, F., Cilia, G., Mancini, S., and Felicioli, A. 2016. Royal Jelly: An ancient remedy with remarkable antibacterial properties. Microbiological research. 192: 130-141. doi: 10.1016/j.micres.2016.06.007.
51. Fujiwara, S., Imai, J., Fujiwara, M., Yaeshima, T., Kawashima, T., and Kobayashi, K. 1990. A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. Journal of biological chemistry. 265(19): 11333-11337. doi: 5;265(19):11333-7.
52. Galeotti, F., Maccari, F., Fachini, A., and Volpi, N. 2018. Chemical composition and antioxidant activity of propolis prepared in different forms and in different solvents useful for finished products. Foods. 7(3): 41. doi: 10.3390/foods7030041.
53. García, M. C., Finola, M. S., and Marioli, J. M. 2010. Antibacterial activity of Royal Jelly against bacteria capable of infecting cutaneous wounds. Journal of ApiProduct and ApiMedical Science. 2(3): 93-99. Doi:10.3896/IBRA.4.02.3.02.
54. Garmani, M.; Koohsari, H.; Seyyed Alangi, S.Z., 2018. The antibactrial and antioxidant activity of several types of beepropolis collected from different geographic regions of Golestan province. Journal of Veterinary Microbiology. 14(2): 25-35.
55. Gebara, E. C. E., Pustiglioni, A. N., de Lima, L. A. P. A., and Mayer, M. P. A. 2003. Propolis extract as an adjuvant to periodontal treatment. Oral health and preventive dentistry. 1(1). PMID: 15643746.
56. Haji Mohammad, F., Koohsari, H., and Ghaboos, S. H. 2022. Antibacterial and antioxidant activity of royal jelly collected from geographical regions with different climates in the north of Iran. Bulgarian Journal of Veterinary Medicine. 25(3): 397-410. doi: 10.15547/bjvm.2020-0133.
57. Hanes, J., and Šimuth, J. 1992. Identification and partial characterization of the major royal jelly protein of the honey bee (Apis mellifera L.). Journal of Apicultural Research. 31(1): 22-26. doi:10.1080/00218839.1992.11101256.
58. Han, S. M., Lee, K. G., and Pak, S.C. 2013. Effects of cosmetics containing purified honeybee (Apis mellifera L.) venom on acne vulgaris. Journal of integrative medicine. 11(5): 320-326. doi: 10.3736/jintegrmed2013043.
59. Han, S., Yeo, J., Baek, H., Lin, S. M., Meyer, S., and Molan, P. 2009. Postantibiotic effect of purified melittin from honeybee (Apis mellifera) venom against Escherichia coli and Staphylococcus aureus. Journal of Asian natural products research. 11(9): 796-804. doi: 10.1080/10286020903164277.
60. Header, E., Hashish, A. E. M., ElSawy, N., Al-Kushi, A., and El-Boshy, M. 2016. Gastroprotective effects of dietary honey against acetylsalicylate induced experimental gastric ulcer in albino rats. Life Science Journal. 13(1): 42-47.
61. Hegazi, A. G., El-Feel, M. A., Abdel-Rahman, E., and Al-Fattah, A. 2015. Antibacterial activity of bee venom collected from Apis mellifera carniolan pure and hybrid races by two collection methods. International Journal of Current Microbiology and Applied Sciences. 4(4): 141-9.
62. Hermanns, R., Mateescu, C., Thrasyvoulou, A., Tananaki, C., Wagener, F. A., and Cremers, N.A. 2020. Defining the standards for medical grade honey. Journal of apicultural research. 59(2): 125-135. doi: 10.1080/00218839.2019.1693713.
63. Hizomi Shirejini, S., Koohsari, H., and Seyed Alangi, S. Z. 2018. Antibacterial activity and physico-chemical analysis of several types of honey with different floral origins in the Golestan province. Iranian Food Science and Technology Research Journal. 14(2): 273-282. DOI: 10.22067/ifstrj.v0i0.60915.
64. Inui, S., Hatano, A., Yoshino, M., Hosoya, T., Shimamura, Y., Masuda, S., ... and Kumazawa, S. 2014. Identification of the phenolic compounds contributing to antibacterial activity in ethanol extracts of Brazilian red propolis. Natural product research. 28(16): 1293-1296. doi: 10.1080/14786419.2014.898146.
65. Issam, A. A., Zimmermann, S., Reichling, J., and Wink, M. 2015. Pharmacological synergism of bee venom and melittin with antibiotics and plant secondary metabolites against multi-drug resistant microbial pathogens. Phytomedicine. 22(2): 245-255. doi: 10.1016/j.phymed.2014.11.019.
66. Jamasbi, E., Batinovic, S., Sharples, R. A., Sani, M. A., Robins-Browne, R. M., Wade, J. D., ... and Hossain, M.A. 2014. Melittin peptides exhibit different activity on different cells and model membranes. Amino acids. 46: 2759-2766. doi: 10.1007/s00726-014-1833-9.
67. Jenkins, R. and Cooper, R. 2012. Improving antibiotic activity against wound pathogens with manuka honey in vitro. PLoS ONE. 2012, 7: e45600. doi: 10.1371/journal.pone.0045600.
68. Kacaniova, M.; Vukovic´, N.; Chlebo, R.; Hašcík, P.; Rovná, K.; Cubon, J., ... and Pasternakiewicz, A. 2012. The antimicrobial activity of honey, bee pollen loads and beeswax from Slovakia. Archives of Biological Sciences. 64: 927–934. doi: 10.2298/ABS1203927K.
69. Kačániová, M., Vatl'ák, A., Vuković, N., Petrová, J., Brindza, J., Nôžková, J., and Fatrcová-Šrámková, K. 2014. Antimicrobial activity of bee collected pollen against clostridia. Animal Science and Biotechnologies, 47(2): 362-365.
70. Karadal, F., Onmaz, N. E., Abay, S., Yildirim, Y., Al, S., Tatyuz, I., and Akcay, A. 2018. A study of antibacterial and antioxidant activities of bee products: Propolis, pollen and honey samples. Ethiopian Journal of Health Development. 32(2).
71. Kaškonienė, V., Adaškevičiūtė, V., Kaškonas, P., Mickienė, R., and Maruška, A. 2020. Antimicrobial and antioxidant activities of natural and fermented bee pollen. Food bioscience. 34 100532. doi: 10.1016/j.fbio.2020.100532.
72. Kharsany, K., Viljoen, A., Leonard, C., and Van Vuuren, S. 2019. The new buzz: Investigating the antimicrobial interactions between bioactive compounds found in South African propolis. Journal of ethnopharmacology. 238: 111867. doi: 10.1016/j.jep.2019.111867.
73. Khider, M., Elbanna, K., Mahmoud, A., and Owayss, A.A. 2013. Egyptian honeybee pollen as antimicrobial, antioxidant agents, and dietary food supplements. Food science and biotechnology. 22: 1-9. doi: 10.1007/s10068-013-0238-y.
74. Khosla, A., Gupta, S. J., Jain, A., Shetty, D. C., and Sharma, N. 2020. Evaluation and comparison of the antimicrobial activity of royal jelly–A holistic healer against periodontopathic bacteria: An: in vitro: study. Journal of Indian Society of Periodontology. 24(3): 221-226. doi: 10.4103/jisp.jisp_486_19.
75. Kilic, A., Baysallar, M., Besırbellıoglu, B., Salıh, B., Sorkun, K. A. D. R. İ. Y. E., and Tanyuksel, M. 2005. In vitro antimicrobial activity of propolis against methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus faecium. 113-117.
76. Kim, H., Park, S. Y., and Lee, G. 2019. Potential therapeutic applications of bee venom on skin disease and its mechanisms: A literature review. Toxins. 11(7): 374. doi: 10.3390/toxins11070374.
77. Koru, O., Toksoy, F., Acikel, C. H., Tunca, Y. M., Baysallar, M., Guclu, A. U., ... and Salih, B. 2007. In vitro antimicrobial activity of propolis samples from different geographical origins against certain oral pathogens. Anaerobe. 13(3-4): 140-145. doi: 10.1016/j.anaerobe.2007.02.001.
78. Kroyer, G., and Hegedus, N. 2001. Evaluation of bioactive properties of pollen extracts as functional dietary food supplement. Innovative Food Science and Emerging Technologies. 2(3): 171-174. doi: 10.1016/S1466-8564(01)00039-X.
79. Kumar, P., Sindhu, R. K., Narayan, S., and Singh, I. 2010. Honey collected from different floras of Chandigarh Tricity: A comparative study involving physicochemical parameters and biochemical activities. Journal of dietary supplements. 7(4): 303-313. doi: 10.3109/19390211.2010.508034.
80. Kuropatnicki, A. K., Szliszka, E., and Krol, W. 2013. Historical aspects of propolis research in modern times. Evidence‐Based Complementary and Alternative Medicine, 2013(1), 964149. doi: 10.1155/2013/964149.
81. Kwakman, P. H., Velde, A. A. T., de Boer, L., Speijer, D., Christina Vandenbroucke‐Grauls, M. J., and Zaat, S.A. 2010. How honey kills bacteria. The FASEB Journal. 24(7): 2576-2582. doi: 10.1096/fj.09-150789.
82. Melliou, E., and Chinou, I. 2005. Chemistry and bioactivity of royal jelly from Greece. Journal of agricultural and food chemistry. 53(23): 8987-8992. doi: 10.1021/jf051550p.
83. Mokaya, H. O., Bargul, J. L., Irungu, J. W., and Lattorff, H. M.G. 2020. Bioactive constituents, in vitro radical scavenging and antibacterial activities of selected Apis mellifera honey from Kenya. International journal of food science and technology. 55(3): 1246-1254. doi: 10.1111/ijfs.14403.
84. Morais, M., Moreira, L., Feás, X., and Estevinho, L.M. 2011. Honeybee-collected pollen from five Portuguese Natural Parks: Palynological origin, phenolic content, antioxidant properties and antimicrobial activity. Food and Chemical Toxicology. 49(5): 1096-1101. doi: 10.1016/j.fct.2011.01.020.
85. Leandro, L. F., Mendes, C. A., Casemiro, L. A., Vinholis, A. H., Cunha, W. R., Almeida, R. D., and Martins, C.H. 2015. Antimicrobial activity of apitoxin, melittin and phospholipase A2 of honey bee (Apis mellifera) venom against oral pathogens. Anais da Academia Brasileira de Ciências. 87(01): 147-155. doi: 10.1590/0001-3765201520130511.
86. Miguel, M. G., Nunes, S., Dandlen, S. A., Cavaco, A. M., and Antunes, M.D. 2010. Phenols and antioxidant activity of hydro-alcoholic extracts of propolis from Algarve, South of Portugal. Food and Chemical Toxicology. 48(12): 3418-3423. doi: 10.1016/j.fct.2010.09.014.
87. Molan, P. C., and Allen, K.L. 1996. The effect of gamma‐irradiation on the antibacterial activity of honey. Journal of pharmacy and pharmacology. 48(11): 1206-1209. doi: 10.1111/j.2042-7158.1996.tb03922.x.
88. Molan, P.C. 1992. The antibacterial activity of honey: 2 Variation in the potency of the antibacterial activity. Bee World. 73(2): 59-76. doi.org/10.1080/0005772X.1992.11099118.
89. Moniruzzaman, M., Khalil, M. I., Sulaiman, S. A., and Gan, S. H. 2013. Physicochemical and antioxidant properties of Malaysian honeys produced by Apis cerana, Apis dorsata and Apis mellifera. BMC Complementary and Alternative Medicine. 13: 1-12. doi: 10.1186/1472-6882-13-43.
90. Nader, R.A.; Mackieh, R.; Wehbe, R.; El Obeid, D.; Sabatier, J.M.; Fajloun, Z. 2021. Beehive Products as Antibacterial Agents: A Review. Antibiotics, 10: 717. https://doi.org/10.3390/antibiotics10060717.
91. Okińczyc, P., Paluch, E., Franiczek, R., Widelski, J., Wojtanowski, K. K., Mroczek, T., ... and Sroka, Z. (2020). Antimicrobial activity of Apis mellifera L. and Trigona sp. propolis from Nepal and its phytochemical analysis. Biomedicine and Pharmacotherapy. 129: 110435. doi: 10.1016/j.biopha.2020.110435.
92. Orsi, R. D. O., Fernandes, A., Bankova, V., and Sforcin, J. M. 2012. The effects of Brazilian and Bulgarian propolis in vitro against Salmonella Typhi and their synergism with antibiotics acting on the ribosome. Natural product research. 26(5): 430-437. doi: 10.1080/14786419.2010.498776.
93. Pucca, M. B., Cerni, F. A., Oliveira, I. S., Jenkins, T. P., Argemí, L., Sørensen, C. V., ... and Laustsen, A.H. 2019. Bee updated: current knowledge on bee venom and bee envenoming therapy. Frontiers in immunology. 10: 2090. doi: 10.3389/fimmu.2019.02090.
94. Ratanavalachai, T., and Wongchai, V. 2002. Antibacterial activity of intact roval jelly, its lipid extract and its defatted extract. Science and Technology Asia. 7: 5-12.
95. Rosmilah, M., Shahnaz, M., Patel, G., Lock, J., Rahman, D., Masita, A., and Noormalin, A. 2008. Characterization of major allergens of royal jelly Apis mellifera. Tropical Biomedicine. 25: 243–251. Doi: ;25(3):243-51.
96. 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): 3236. doi.org/10.3390/molecules23123236.
97. Seibert, J. B., Bautista-Silva, J. P., Amparo, T. R., Petit, A., Pervier, P., dos Santos Almeida, J. C., ... and Dos Santos, O.D.H. 2019. Development of propolis nanoemulsion with antioxidant and antimicrobial activity for use as a potential natural preservative. Food chemistry. 287: 61-67. doi: 10.1016/j.foodchem.2019.02.078.
98. Seidel, V., Peyfoon, E., Watson, D. G., and Fearnley, J. 2008. Comparative study of the antibacterial activity of propolis from different geographical and climatic zones. Phytotherapy research. 22(9): 1256-1263. doi: 10.1002/ptr.2480.
99. Shabbir, A., Rashid, M., and Tipu, H.N. 2016. Propolis, a hope for the future in treating resistant periodontal pathogens. Cureus. 8(7): e682. doi: 10.7759/cureus.682.
100. Shakiba, E., Koohsari, H., and Mahmoodjanloo, M.A. 2018. Antibacterial Activity of Honey Bee Products Collected from Three Different Climate in Golestan Province in Northern Iran. International Journal of Molecular and Clinical Microbiology. 8(2): 1062-1073.
101. Shen LiRong, S. L., Liu DanDan, L. D., Li MeiLu, L. M., Jin Feng, J. F., Din MeiHui, D. M., Parnell, L. D., and Lai, C.Q. 2012. Mechanism of action of recombinant Acc-royalisin from royal jelly of Asian honeybee against Gram-positive bacteria. PLoS ONE. 7: e47194. doi: 10.1371/journal.pone.0047194.
102. Šimunovic, K.; Abramovi, H.; Lilek, N.; Angelova, M.; Podržaj, L.; Smole Možina, S.S. 2019. Microbiological quality, antioxidantive and antimicrobial properties of Slovenian bee pollen. Agrofor, 4(1). 4: 82–92. doi: 10.7251/AGRENG1901082S.
103. Sowa, P., Grabek‐Lejko, D., Wesołowska, M., Swacha, S., and Dżugan, M. 2017. Hydrogen peroxide‐dependent antibacterial action of Melilotus albus honey. Letters in applied microbiology. 65(1): 82-89. doi: 10.1111/lam.12749.
104. Szweda, P. 2017. Antimicrobial Activity of Honey. Honey analysis. Croatia, Intech, Open. 17: 216-228. doi: 10.5772/67117.
105. Taha, E. K. A., Al-Kahtani, S., and Taha, R. 2019. Protein content and amino acids composition of bee-pollens from major floral sources in Al-Ahsa, eastern Saudi Arabia. Saudi Journal of Biological Sciences. 26(2): 232-237. doi: 10.1016/j.sjbs.2017.06.003.
106. Veiga, R. S., De Mendonça, S., Mendes, P. B., Paulino, N., Mimica, M. J., Lagareiro Netto, A. A., ... and Marcucci, M. C. 2017. Artepillin C and phenolic compounds responsible for antimicrobial and antioxidant activity of green propolis and Baccharis dracunculifolia DC. Journal of Applied Microbiology. 122(4): 911-920. doi: 10.1111/jam.13400.
107. Velásquez, P., Rodriguez, K., Retamal, M., Giordano Villatoro, A., Valenzuela Roediger, L. M., and Montenegro Rizzardini, G. 2017. Relation between composition, antioxidant and antibacterial activities and botanical origin of multi-floral bee pollen. Journal of Applied Botany and Food Quality. 90: 306–314.
108. Veloz, J. J., Alvear, M., and Salazar, L. A. 2019. Antimicrobial and antibiofilm activity against Streptococcus mutans of individual and mixtures of the main polyphenolic compounds found in Chilean propolis. BioMed research international. 2019(1): 7602343. doi: 10.1155/2019/7602343.
109. Wang, L., Zhao, X., Zhu, C., Zhao, Y., Liu, S., Xia, X., ... and Hu, J. 2020. The antimicrobial peptide MPX kills Actinobacillus pleuropneumoniae and reduces its pathogenicity in mice. Veterinary microbiology. 243: 108634. doi: 10.1016/j.vetmic.2020.108634.
110. Wehbe, R., Frangieh, J., Rima, M., El Obeid, D., Sabatier, J. M., and Fajloun, Z. 2019. Bee venom: Overview of main compounds and bioactivities for therapeutic interests. Molecules. 24(16): 2997. doi: 10.3390/molecules24162997.
111. Wilkinson, J. M., and Cavanagh, H. M. 2005. Antibacterial activity of 13 honeys against Escherichia coli and Pseudomonas aeruginosa. Journal of medicinal food. 8(1): 100-103. doi: 10.1089/jmf.2005.8.100.
112. Wojtyczka, R. D., Dziedzic, A., Idzik, D., Kępa, M., Kubina, R., Kabała-Dzik, A., ... and Wąsik, T. J. 2013. Susceptibility of Staphylococcus aureus clinical isolates to propolis extract alone or in combination with antimicrobial drugs. Molecules. 18(8): 9623-9640. doi: 10.3390/molecules18089623.
113. Wu, X., Singh, A. K., Wu, X., Lyu, Y., Bhunia, A. K., and Narsimhan, G. 2016. Characterization of antimicrobial activity against Listeria and cytotoxicity of native melittin and its mutant variants. Colloids and Surfaces B: Biointerfaces. 143: 194-205. doi: 10.1016/j.colsurfb.2016.03.037.
114. Yacoub, T., Rima, M., Karam, M., Sabatier, J. M., and Fajloun, Z. 2020. Antimicrobials from venomous animals: An overview. Molecules. 25(10): 2402. doi: 10.3390/molecules25102402.
115. Yazdani, Amin; Koohsari, Hadi; Sadegh Shesh Poli, Maryam. Antibacterial Activity of Honey and Bee Pollen Collected from Bee Hives from Three Climatic Regions of Golestan Province Against some Clinical Isolates with High Antibiotic Resistance. Research and Innovation in Food Science and Technology. 2024. doi: 10.22101/jrifst.2024.415662.1514.
116. Yoshimasu, Y., Ikeda, T., Sakai, N., Yagi, A., Hirayama, S., Morinaga, Y., ... and Nakao, R. 2018. Rapid bactericidal action of propolis against Porphyromonas gingivalis. Journal of dental research. 97(8): 928-936. doi: 10.1177/0022034518758034.
117. Yousaf, I., Ishaq, I., Hussain, M. B., Inaam, S., Saleem, S., and Qamar, M. U. 2019. Antibacterial activity of Pakistani Beri honey compared with silver sulfadiazine on infected wounds: a clinical trial. Journal of Wound Care. 28(5): 291-296. doi: 10.12968/jowc.2019.28.5.291.
