ANTIMICROBIAL ACTIVITY OF EGYPTIAN SIDR HONEY AND ITS SYNERGISTIC ACTION WITH ANTIMICROBIAL AGENTS

Year 2023, , 1 - 13, 19.05.2023

Nageh Omran Mostafa Hassan , Mohamed Abdel-rahman Abdel-aleem Desoky Stayed Hamouda

https://doi.org/10.31467/uluaricilik.1170635

Abstract

Determine the in vitro antibacterial potential activity sidr honey produced in upper Egypt against five references bacterial strains (Gram positive and Gram negative strains) and its synergistic effect with some antimicrobial agents. Material & Methods: fifteen Sidr honey samples were collected from three Governorates in Upper Egypt. Honey samples were diluted and tested against Staphylococcus aureus, Streptococcus agalactiae, Escherichia coli, Klebsiella pneumoniae and Bacillus cereus by agar dilution method. Post determination of the minimum inhibitory concentration (MIC) values, six honey samples were examined for their synergistic action with the ineffective antimicrobial agents. Results: In vitro antimicrobial sensitivity test, all bacterial strains showed multidrug resistance action against the 13 tested antimicrobial agents with high multiple antibiotic resistance (MAR) index, it was ≥ 0.38. All Sidr bee honey samples showing antibacterial activity against the five tested references bacterial strains. All Sidr bee honey samples, showed better synergistic effect with all antimicrobial agents against.

Keywords

Egyptian Sidr honey, Antimicrobial impact, Minimum inhibitory concentration, Synergistic effect

Supporting Institution

No

Mısır Sidr Balının Antimikrobiyal Aktivitesi ve Antimikrobiyal Ajanlarla Sinerjik Etkisi

Abstract

Bu çalışmanın amacı, Yukarı Mısır'da üretilen Sidr balının beş referans bakteri suşuna (Gram pozitif ve Gram negatif suşlar) karşı in vitro antibakteriyel potansiyel aktivitesini ve bazı antimikrobiyal ajanlarla sinerjistik etkisini belirlemektir. Yukarı Mısır'daki üç valilikten on beş Sidr balı örneği toplanmıştır. Bal örnekleri seyreltilmiş ve agar seyreltme yöntemiyle Staphylococcus aureus, Streptococcus agalactiae, Escherichia coli, Klebsiella pneumoniae ve Bacillus cereus'a karşı test edilmiştir. Minimum inhibitör konsantrasyon (MİK) değerlerinin belirlenmesinden sonra, altı bal örneği etkisiz antimikrobiyal ajanlarla sinerjik etkileri açısından incelenmiştir. In vitro antimikrobiyal duyarlılık testinde, tüm bakteri suşları test edilen 13 antimikrobiyal ajana karşı yüksek çoklu antibiyotik direnci (MAR) indeksi ile çoklu ilaç direnci etkisi göstermiştir, bu değer ≥ 0.38'dir. Tüm Sidr arı balı örnekleri, test edilen beş referans bakteri suşuna karşı antibakteriyel aktivite göstermiştir. Tüm Sidr arı balı örnekleri, tüm antimikrobiyal ajanlara karşı daha iyi sinerjik etki göstermiştir.

Keywords

Mısır Sidr balı, Antimikrobiyal etki, Minimum inhibitör konsantrasyon, Sinerjistik etki

References

• Abdul-Hafeez, MM., Hamouda, SM and Abd El Rahman, MF. Synergistic antimicrobial effect of Egyptian honey with antibiotics and its capability to restore MRSA sensitive to oxacillin. International Journal of Science and Research. 2021; 10 (3):1389-1395. DOI: 10.21275/SR21313001535.
• Almasaudi, BS, Alaa, AM, Al-Nahari, El, Sayed M. Antimicrobial effect of different types of honey on Staphylococcus aureus. Saudi Journal of Biological Sciences. 2017; 24:1255–1261.
• Almasaudi, BS. The antibacterial activities of honey. Saudi Journal of Biological Sciences. 2021;28: 2188–2196. doi: 10.1016/j.sjbs.2020.10.017.
• Alqurashi, AM, Masoud, EA, Alamin, MA. Antibacterial activity of Saudi honey against Gram negative bacteria. J. of Microbiology and Antimicrobials. 2013; 5(1):1- 5. DOI: 10.5897/JMA2012.0235.
• Alzahrani, HA, Alsabehi R, Boukraâ L, Abdellah F, Bellik Y. Antibacterial and antioxidant potency of floral honeys from different botanical and geographical origins. Molecules. 2012; 17: 10540-10549. doi: 10.3390/molecules170910540.
• Blair, S, Cokcetin, N, Harry E, Carter, D. The unusual antibacterial activity of medical-grade Leptospermum honey: antibacterial spectrum, resistance and transcriptome analysis. European journal of clinical microbiology & infectious diseases. 2009; 28: 1199–1208. doi: 10.1007/s10096-009-0763.
• Braide, W, Oranusi, S, Akaluka, C. Antibacterial efficacy of crude and diluted honey on four wound isolates. Global Advanced Research J. of Microbiology. 2012; 1(1): 1–4.
• Brown, HL, Georgie, M, Matthew, D. Antibacterial and antivirulence activity of Manuka Honey against genetically diverse Staphylococcus pseudintermedius strains. Applied and Environmental Microbiology. 2020; 86 (20): e01768-20.
• Brudzynsk, K. Honey as an Ecological Reservoir of Antibacterial Compounds Produced by Antagonistic Microbial Interactions in Plant Nectars, Honey and Honey Bee. Antibiotics. 2021; 10: 551. doi: 10.3390/antibiotics10050551.
• Bucekova, M, Martin S, Ivana V. Bee-derived antibacterial peptide, efensing-1, promotes wound reepithelialisation in vitro and in vivo. Scientific Reports. 2017; 7: 7340. doi:10.1038/s41598-017-07494-0.
• Cooper, R, Jenkins, L, Henriques, AFM, Duggan, R, Burton, N. Absence of bacterial resistance to medical-grade manuka honey. European j. of clinical microbiology & infectious diseases. 2010; 1–5. doi: 10.1007/s10096-010-0992.
• Cooper, RA, Molan, PC, Harding, KG. The sensitivity to honey of Gram-positive cocci of clinical significance isolated from wounds. J. Appl. Microbiol. 2002; 93(5): 857-863. doi:org/10.1046/i.1365-2672.2002.01761.x
• Da Silva, PM, Gauche, C, Gonzaga, LV, Costa, ACO, Fett R. “Honey: Chemical Composition, Stability and Authenticity” in Food Chemistry. 2016; 196: 309-323. doi: 10.1016/j.foodchem.2015.09.051.
• Dash, N, Debadatta, P, Mansour, Al-Zarouni. Antimicrobial Effect of Honey from the Arabian Gulf Region against Bacterial Isolates from Pus and Wound swabs. Advances in Microbiology. 2016; 6: 745-752. DOI: 10.4236/aim.2016.610073
• Elbanna, K, Attalla, K, Elbadry, M, Abdeltawab, A, Gamal-Eldin, H, Ramadan, MF. Impact of floral sources and processing on the antimicrobial activities of different unifloral honeys. Asian Pacific Journal of Tropical Disease. 2014; 4(3): 194–200. doi: 10.1016/S2222-1808(14)60504-1.
• Eman, MH, Mohammed, MS. Shaoka and Sidr honeys surpass in their antibacterial activity local and imported honeys available in Saudi markets against pathogenic and food spoilage bacteria. Australian Journal of Basic and Applied Sciences. 2011; 5(4): 187-191.
• Enany, M E, Algammal, AM, Shagar, GI. Molecular typing and evaluation of Sidr honey inhibitory effect on virulence genes of MRSA strains isolated from catfish in Egypt. Pak. J. Pharm. Sci. 2018; 31, (5):1865-1870.
• European Center for Disease Prevention and Control (ECDCE). The bacterial challenge: time to react. Stockholm: European Center for Disease Prevention and Control. 2009.
• Go´rniak, I, Rafał, B, Jarosław, K. Comprehensive review of antimicrobial activities of plant flavonoids. Phytochem Rev. 2019; 18:241–272. doi10.1007/s11101-018-9591.
• Hamouda, SM, Heba, MMK, Mahmoud, A, Magda, MA, Haroun, AY. Apitherapy of Septic Metacarpal and Metatarsal Wounds (An Experimental Study on Donkeys). Clinical Medicine Research. 2019; 8(4): 77-84. doi:10.11648/j.cmr.20190804.12.
• Hegazi, AG, Abd Allah, FM. Antimicrobial activity of different Saudi Arabia honeys. Global Veterinaria. 2012; 9(1): 53–59.
• Hegazi, AG, Al Guthami, FM, Al Gethami, AFM. Potential antibacterial activity of some Saudi Arabia honey. Veterinary World. 2017; 10(2): 233-237. DOI:10.14202/vetworld.2017.233-237.
• Hegazi, AG. Antimicrobial activity of different Egyptian honeys as comparison of Saudi Arabia honey. Res J Microbiol. 2011; 6:488–495. doi: 10.17311/jm.2011.488.495.
• Irish, J, Blair, S, Carter, DA. The antibacterial activity of honey derived from Australian flora. PLoS ONE. 2011; 6(3): e18229. https ://doi. org/10.1371/journ al.pone.0018229.
• Jaktaji, PR, Ghalamfarsa, F. Antibacterial activity of honeys and potential synergism of honeys with antibiotics and alkaloid extract of Sophora alopecuroides plant against antibiotic-resistant Escherichia coli mutant. Iran J Basic Med Sci. 2021; 24(5):623-628. doi: 10.22038/ijbms.2021.54224.12179.
• Jenkins, R, Burton, N, Cooper, R. Proteomic and genomic analysis of methicillin resistant Staphylococcus aureus (MRSA) exposed to manuka honey in vitro demonstrated down-regulation of virulence markers. J. Antimicrob. Chemother.2014; 9(3):603-615. doi: 0.1093/jac/dkt430.
• Jenkins, RE, Cooper, R. Synergy between oxacillin and manuka honey sensitizes methicillin-resistant Staphylococcus aureus to oxacillin. J. Antimicrob. Chemother. 2012; 67:1405–1407. DOI:10.1093/jac/dks071.
• Liu, M, Lu, J, Müller, P. Antibiotic specific differences in the response of Staphylococcus aureus to treatment with antimicrobials combined with manuka honey. Frontiers in microbiology. 2015; 5 (Article 779):1-9. doi:10. 3389 / fmicb. 00779.
• Liu, MY, Nural C, Jing L. Rifampicin - Manuka honey combinations are superior to other antibiotic-Manuka honey combinations in eradicating Staphylococcus aureus Biofilms. FrontiesMicrobiol.2018; 8(11):1-12.doi.org/10.3389/fmicb.2017.02653.
• Louveaux J, Maurizio A. and Vorwohl, G. Methods of melissopalynology. Bee World. 1978; 59:139-157.
• Mandal, MD, Mandal, S. Honey: its medicinal property and antibacterial activity. Asian Pacific Journal of Tropical Biomedicine. 2012; 1(2): 154-160.
• Masoud, EA, Alqurashi, AM, Alamin, AA. Synergistic effects of honeys and commonly used antibiotics on Gram Positive Bacteria. Egypt. Acad. J. Biolog. Sci. 2015; 7(1): 101–109. DOI:10.21608/eajbsg.2015.16491.
• Mohammad, A, Al-Kafaween, MHA, Hamid ANA. Potential antibacterial activity of Yemeni Sidr honey against Pseudomonas aeruginosa and Streptococcus pyogenes. Anti-Infective Agents in Medicinal Chemistry. 2021;19(4):1-15.DOI:10.2174/2211352519666210319100204.
• Mohammed, AAA, Sailh, MK, Ali AF, Nusaybah, KHS. In Vitro antibacterial activity of some natural and trade iraqi honey against MRSA Staphylococcus Heamolyticus isolated from some burned patients in Misan City. American Journal of Microbiological Research. 2016; 4(5): 159-163. DOI:10.12691/AJMR-4-5-6.
• Mohammed, AS, Jayashankar, M. Evaluation of antibacterial activity of some Indian and Yemeni honey against few bacterial isolates from human patients. Egypt. J. Microbiol. 2020; 55: 21-28. doi: 10.21608/EJM.2020.1135.
• Molan, PC, Cooper, RA. Honey and sugar as a dressing for wounds and ulcers. Trop. Doct. 2000; 30:249-250. doi: 10.1177/004947550003000101.
• Müller, P, Alber, DG, Turnbull, L. Synergism between Medihoney and Rifampicin against Methicillin-Resistant Staphylococcus aureus (MRSA). PLOS ONE. 2013; 8(2): doi: 10.1371/journal.pone.0057679.
• National Committee for Laboratory Standards (NCCLS) 2000. Performance Standards for Antimicrobial Disk Susceptibility Test. Approved Standard M2 – A7, M100 – S10. PA.
• Owayss AA, Khaled E, Javaid I. In vitro antimicrobial activities of Saudi honeys originating from Ziziphus spina-christi L. and Acacia gerrardii Benth. Trees. Food Sci. Nutr. 2019; 8:390–401. doi: org/10.1002/fsn3.1320.
• Quinn PJ, Carter ME, Markey B, Carter GR. Bacteriology: Clinical veterinary microbiology. 2004; (6thEd.) Mosby Edinburgh London New York Oxford Philadelphia St Louis Sydney Toronto.
• Sayed, MS, Maryam FM, El Berbawy SM. Bacteriological studies on sub-clinical mastitis in cows and buffaloes with trails for its treatment. Assiut Veterinary Medical Journal. 2011; 57, (129):185-200. doi:10.21608/AVMJ.2011.174542.
• Scripcă, LA, Liliana N, Sonia A. Comparison of physicochemical, microbiological properties and bioactive compounds content of grassland honey and other floral origin honeys. Molecules. 2019; 24:1-17, 2932. doi:10.3390/molecules24162932.
• Stagos, D, Soulitsiotis, N, Tsadila, C. Antibacterial and antioxidant activity of different types of honey derived from Mount Olympus in Greece. International Journal of Molecular Medicine. 2018; 42(2):726–734. doi:10.3892/ijmm.2018.3656.
• Stepanović S, Antić N, Dakić I. In vitro antimicrobial activity of propolis and synergism between propolis and antimicrobial drugs. Microbiol. Res. 2003; 158(4):353-357. doi:10.1078/0944-5013-00215.
• Subramani, S, Vignesh, S. MAR index study and MDR character analysis of a few golden Staph isolates. Asian Journal of Pharmacy and Life Science. 2012; 2(2).
• Szweda, P. Antimicrobial Activity of Honey. Honey Analysis. 2017; pp. 215-232. doi:10.1155/2019/2464507.
• Zainol, MI, Kamaruddin, MY, Mohd, YMY. Antibacterial activity of selected Malaysian honey. BMC Complementary and Alternative Medicine. 2013; 13:129.