Original Article

A comparative study of antibacterial and antivirulence activities of four selected honeys to Manuka honey

Abstract

Background and Objectives: Honey has excellent antibacterial properties against various microorganisms of several different species. To date, there is no comparative evaluation of the antibacterial activity of Jarrah honey (JH), Kelulut Madu honey (KMH), Gelam honey (GH), and Acacia honey (AH) with that of Manuka honey (MH). The purpose of this study was to conduct such study and to compare the antibacterial activity of JH, KMH, GH, and AH with that of MH against Pseudomonas aeruginosa and Streptococcus pyogenes.
Materials and Methods: Activity was assessed using broth microdilution, time kill viability, microtiter plate, scanning electron microscope (SEM) and Quantitative Real-Time Polymerase Chain Reaction (RT-qPCR).
Results: The susceptibility tests revealed promising antibacterial activities of all honeys against both bacteria. The MICs of JH, KMH, GH, and AH ranged from 20% to 25% compared to MH (12.5%) against both bacteria. The MBCs of JH, KMH, GH, and AH ranged from 20% to 50% compared to MH (20%) against both bacteria. Treatment of both bacteria with 2× MIC (Minimum inhibitory concentration) of MH, JH, KMH, GH, and AH for 9 hours resulted in reduction in colony-forming unit (CFU/ml). SEM images showed that the morphological changes, cell destruction, cell lysis and biofilm disruption in both bacteria after exposure to all honeys. RT-qPCR analysis revealed that the expression of all genes in both bacteria were downregulated following treatment with all honeys. Among the all-tested honeys, MH showed the highest total antibacterial and antivirulence activities.
Conclusion: Our results indicate that all honeys activity included inhibition of both bacteria due to a decrease in expression of essential genes associated with both bacteria, suggesting that all honeys could potentially be used as an alternative therapeutic agent against certain microorganisms particularly against P. aeruginosa and S. pyogenes.

1. Al-Bakri AG, Mahmoud NN. Photothermal-induced antibacterial activity of gold nanorods loaded into polymeric hydrogel against Pseudomonas aeruginosa biofilm. Molecules 2019;24:2661.
2. Jamal M, Ahmad W, Andleeb S, Jalil F, Imran M, Nawaz MA, et al. Bacterial biofilm and associated infections. J Chin Med Assoc 2018;81:7-11.
3. Dhingra S, Rahman NAA, Peile E, Rahman M, Sartelli M, Hassali MA, et al. Microbial resistance movements: an overview of global public health threats posed by antimicrobial resistance, and how best to counter. Front Public Health 2020;8: 535668.
4. Jolivet-Gougeon A, Bonnaure-Mallet M. Biofilms as a mechanism of bacterial resistance. Drug Discov Today Technol 2014;11:49-56.
5. Pang Z, Raudonis R, Glick BR, Lin TJ, Cheng Z. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and alternative therapeutic strategies. Biotechnol Adv 2019;37:177-192.
6. Wasfi R, Elkhatib WF, Khairalla AS. Effects of selected Egyptian honeys on the cellular ultrastructure and the gene expression profile of Escherichia coli. PLoS One 2016;11 (3):e0150984.
7. Pećanac M, Janjić Z, Komarčević A, Pajić M, Dobanovački D, Mišković SS. Burns treatment in ancient times. Med Pregl 2013;66:263-267.
8. Mavric E, Wittmann S, Barth G, Henle T. Identification and quantification of methylglyoxal as the dominant antibacterial constituent of Manuka (Leptospermum scoparium) honeys from New Zealand. Mol Nutr Food Res 2008;52:483-489.
9. Tsuruda JM, Chakrabarti P, Sagili RR. Honey bee nutrition. Vet Clin North Am Food Anim Pract 2021;37:505-519.
10. Anthimidou E, Mossialos D. Antibacterial activity of Greek and Cypriot honeys against Staphylococcus aureus and Pseudomonas aeruginosa in comparison to manuka honey. J Med Food 2013;16:42-47.
11. Ng WJ, Ken KW, Kumar RV, Gunasagaran H, Chandramogan V, Lee YY. In-vitro screening of Malaysian honey from different floral sources for antibacterial activity on human pathogenic bacteria. Afr J Tradit Complement Altern Med 2014;11:315-318.
12. 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;69:603-615.
13. Al-kafaween MA, Al-Jamal HAN, Hilmi ABM, Elsahoryi NA, Jaffar N, Zahri MK. Antibacterial properties of selected Malaysian Tualang honey against Pseudomonas aeruginosa and Streptococcus pyogenes. Iran J Microbiol 2020;12:565-576.
14. Zainol MI, Mohd Yusoff K, Mohd Yusof MY.. Antibacterial activity of selected Malaysian honey. BMC Complement Altern Med 2013;13:129.
15. Tarawneh O, Abu Mahfouz H, Hamadneh L, Deeb AA, Al-Sheikh I, Alwahsh W, et al. Assessment of persistent antimicrobial and anti-biofilm activity of p-HEMA hydrogel loaded with rifampicin and cefixime. Sci Rep 2022;12:3900.
16. Roberts AE, Maddocks SE, Cooper RA. Manuka honey reduces the motility of Pseudomonas aeruginosa by suppression of flagella-associated genes. J Antimicrob Chemother 2015;70:716-725.
17. Jarrar YB, Jarrar Q, Abaalkhail SJ, Moh'd Kalloush H, Naser W, Zihlif M, et al. Molecular toxicological alterations in the mouse hearts induced by sub-chronic thiazolidinedione drugs administration. Fundam Clin Pharmacol 2022;36:143-149.
18. Jarrar Y, Jarrar Q, Abu-Shalhoob M, Abed A, Sha'ban E. Relative expression of mouse Udp-glucuronosyl transferase 2b1 gene in the livers, kidneys, and hearts: the influence of nonsteroidal anti-inflammatory drug treatment. Curr Drug Metab 2019;20:918-923.
19. A Al-Kafaween M, Mohd Hilmi AB, Al-Jamal HAN, A Elsahoryi N, Jaffar N, Zahri MK. Pseudomonas aeruginosa and Streptococcus pyogenes exposed to Malaysian Trigona honey in vitro demonstrated downregulation of virulence factor. Iran J Biotechnol 2020;18 (4):e2542.
20. Cornara L, Biagi M, Xiao J, Burlando B. Therapeutic properties of bioactive compounds from different honeybee products. Front Pharmacol 2017;8:412.
21. Almasaudi S. The antibacterial activities of honey. Saudi J Biol Sci 2021;28:2188-2196.
22. Albaridi NA. Antibacterial potency of honey. Int J Microbiol 2019;2019:2464507.
23. Bang LM, Buntting C, Molan P. The effect of dilution on the rate of hydrogen peroxide production in honey and its implications for wound healing. J Altern Complement Med 2003;9:267-273.
24. Molan PC. The antibacterial activity of honey: 1. The nature of the antibacterial activity. Bee world 1992;73:5-28.
25. Zainol MI, Mohd Yusoff K, Mohd Yusof MY. Antibacterial activity of selected Malaysian honey. BMC Complement Altern Med 2013;13:129.
26. Abbas HA. Comparative antibacterial and antibiofilm activities of manuka honey and Egyptian clover honey. Asian J Appl Sci 2014;2:110-115.
27. Bouacha M, Ayed H, Grara N. Honey bee as alternative medicine to treat eleven multidrug-resistant bacteria causing urinary tract infection during pregnancy. Sci Pharm 2018;86:14.
28. Shenoy VP, Ballal M, Shivananda P, Bairy I. Honey as an antimicrobial agent against Pseudomonas aeruginosa isolated from infected wounds. J Glob Infect Dis 2012;4:102-105.
29. Maddocks SE, Lopez MS, Rowlands RS, Cooper RA. Manuka honey inhibits the development of Streptococcus pyogenes biofilms and causes reduced expression of two fibronectin binding proteins. Microbiology (Reading) 2012;158:781-790.
30. Mandal MD, Mandal S. Honey: its medicinal property and antibacterial activity. Asian Pac J Trop Biomed 2011;1:154-160.
31. Roberts AEL, Maddocks SE, Cooper RA. Manuka honey is bactericidal against Pseudomonas aeruginosa and results in differential expression of oprF and algD. Microbiology (Reading) 2012;158:3005-3013.
32. Boorn KL, Khor YY, Sweetman E, Tan F, Heard TA, Hammer KA. Antimicrobial activity of honey from the stingless bee Trigona carbonaria determined by agar diffusion, agar dilution, broth microdilution and time‐kill methodology. J Appl Microbiol 2010;108:1534-1543.
33. Henriques AF, Jenkins RE, Burton NF, Cooper RA. The effect of manuka honey on the structure of Pseudomonas aeruginosa. Eur J Clin Microbiol Infect Dis 2011;30:167-171.
34. Zakaria AS. Mechanism of antibacterial action of honey on pathogenic wound bacterial strains: A proteomic analysis. Int Res J Pharm 2015;6:778-788.
35. Proaño A, Coello D, Villacrés-Granda I, Ballesteros I, Debut A, Vizuete K. The osmotic action of sugar combined with hydrogen peroxide and bee-derived antibacterial peptide Defensin-1 is crucial for the antibiofilm activity of eucalyptus honey. LWT 2021;136:110379.
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IssueVol 14 No 2 (2022) QRcode
SectionOriginal Article(s)
DOI https://doi.org/10.18502/ijm.v14i2.9193
Keywords
Honey; Pseudomonas aeruginosa; Streptococcus pyogenes; Gene expression profiling; Real-time polymerase chain reaction

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How to Cite
1.
Al-kafaween M, Nagi Al-Jamal H. A comparative study of antibacterial and antivirulence activities of four selected honeys to Manuka honey. Iran J Microbiol. 2022;14(2):238-251.