Comparison of the antimicrobial and antivirulence activities of Sidr and Tualang honeys with Manuka honey against Staphylococcus aureus
Abstract
Background and Objectives: Honey is one of the oldest traditional remedies that has been widely utilized to cure a variety of human ailments. The objective of this research was to test and compare the antibacterial activity of Sidr honey (SH) and Tualang honey (TH) to that of Manuka honey (MH) against Staphylococcus aureus.
Materials and Methods: The antibacterial activity of MH, SH and TH against S. aureus was investigated by agar well diffusion, Minimum Inhibitory Concentration (MIC), Minimum Bactericidal Concentration (MBC), time-kill curve, microtiter plate and RT-qPCR analysis.
Results: Agar inhibition assay showed that MH possess highest total antibacterial activity against S. aureus with an inhibition zone 25.1 mm compared with that of SH (22.2 mm) and TH (21.3 mm). The findings showed that when compared to SH and TH (MIC: 25% and MBC: 50%), MH honey had the lowest MIC (12.5%) and MBC (25%). After S. aureus was exposed to MH, SH, and TH, there was a decrease in colony-forming unit as seen by the time-kill curve. The lowest concentration 20% of MH, SH and TH was significantly found to inhibit S. aureus biofilm. The RT-qPCR results revealed that all the selected genes in S. aureus were downregulated in gene expression following exposure to each of the tested honeys. Comparing the total antibacterial, antibiofilm, and antivirulence activities of all the tested honeys, MH demonstrated the greatest levels of these properties.
Conclusion: According to this study, various types of each evaluated honey have the capacity to effectively suppress and modify the virulence of S. aureus via a variety of molecular targets.
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11. Zulkhairi Amin FA, Sabri S, Mohammad SM, Ismail M, Chan KW, Ismail N, et al. Therapeutic properties of stingless bee honey in comparison with european bee honey. Adv Pharmacol Sci 2018; 2018: 6179596.
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14. Zainol MI, Mohd Yusoff K, Mohd Yusof MY. Antibacterial activity of selected Malaysian honey. BMC
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15. Al-kafaween MA, Mohd Hilmi AB, Al-Jamal HAN, Al-Groom RM, Elsahoryi NA, Al-Sayyed H. Potential Antibacterial activity of Yemeni Sidr Honey against Pseudomonas aeruginosa and Streptococcus pyogenes. Anti-Infect Agents 2021; 19: 1-15.
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19. 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.
20. 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.
21. Al-kafaween MA, Kafaween H, Al-Groom RM. A comparative study of antibacterial activity of Citrus and Jabali honeys with Manuka honey. Appl Environ Biotechnol 2022; 7: 28-37.
22. Al-Kafaween MA, Hilmi AB, Al-Jamal HA. The beneficial effects of stingless Bee Kelulut honey against Pseudomonas aeruginosa and Streptococcus pyogenes planktonic and biofilm. Trop J Nat Prod Res 2021; 5: 1788-1796.
23. Huwaitat R, Coulter SM, Porter SL, Pentlavalli S, Laverty G. Antibacterial and antibiofilm efficacy of synthetic polymyxin‐mimetic lipopeptides. Pept Sci 2020; 113(1): e24188.
24. 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.
25. 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.
26. Sherlock O, Dolan A, Athman R, Power A, Gethin G, Cowman S, et al. Comparison of the antimicrobial activity of Ulmo honey from Chile and Manuka honey against methicillin-resistant Staphylococcus aureus, Escherichia coli and Pseudomonas aeruginosa. BMC Complement Altern Med 2010; 10: 47.
27. Alkhyat SH, Al-Maqtari M. Effectiveness of antibiotics blended with honey on some pathogenic bacteria species. Int J Microbiol Immunol Res 2014; 2: 109-115.
28. Al-Kafaween MA, Al-Jamal HAN. A comparative study of antibacterial and antivirulence activities of four selected honeys to Manuka honey. Iran J Microbiol 2022; 14: 238-251.
29. 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.
30. Tan HT, Rahman RA, Gan SH, Halim AS, Hassan SA, Sulaiman SA, et al. The antibacterial properties of Malaysian tualang honey against wound and enteric microorganisms in comparison to manuka honey. BMC Complement Altern Med 2009; 9: 34.
31. Singleton P. Bacteria in biology, biotechnology and medicine 6th edition. Wiley 2004. pp1-526.
32. Lu J, Cokcetin NN, Burke CM, Turnbull L, Liu M, Carter DA, et al. Honey can inhibit and eliminate biofilms produced by Pseudomonas aeruginosa. Sci Rep 2019; 9: 18160.
33. Roberts AEL (2014). The inhibition of Pseudomonas aeruginosa by manuka honey.
34. Grecka K, Kuś PM, Worobo RW, Szweda P. Study of the anti-staphylococcal potential of honeys produced in Northern Poland. Molecules 2018; 23: 260.
35. 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.
36. Lu J, Turnbull L, Burke CM, Liu M, Carter DA, Schlothauer RC, et al. Manuka-type honeys can eradicate biofilms produced by Staphylococcus aureus strains with different biofilm-forming abilities. PeerJ 2014; 2: e326.
37. 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.
38. Ahmed AA, Salih FA. Low concentrations of local honey modulate Exotoxin A expression, and quorum sensing related virulence in drug-resistant Pseudomonas aeruginosa recovered from infected burn wounds. Iran J Basic Med Sci 2019; 22: 568-575.
39. Proaño A, Coello D, Villacrés-Granda I, Ballesteros I, Debut A, Vizuete K, et al. 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.
2. Krishnakumar GS, Mahendiran B, Gopalakrishnan S, Muthusamy S, Malarkodi Elangovan S. Honey based treatment strategies for infected wounds and burns: A systematic review of recent pre-clinical research. Wound Med 2020; 30: 100188.
3. Adebolu TT. Effect of natural honey on local isolates of diarrhea-causing bacteria in southwestern Nigeria. Afr J Biotechnol 2005; 4: 1172-1174.
4. Eteraf-Oskouei T, Najafi M. Traditional and modern uses of natural honey in human diseases: a review. Iran J Basic Med Sci 2013; 16: 731-742.
5. Vallianou NG, Gounari P, Skourtis A, Panagos J, Kazazis C. Honey and its anti-inflammatory, anti-bacterial and anti-oxidant properties. Gen Med 2014; 2: 1-5.
6. Lan X, Wang W, Li Q, Wang J. The natural flavonoid pinocembrin: molecular targets and potential therapeutic applications. Mol Neurobiol 2016; 53: 1794-1801.
7. Lay-Flurrie K. Honey in wound care: effects, clinical application and patient benefit. Br J Nurs 2008; 17: S30, S32-6.
8. Brudzynski K, Abubaker K, St-Martin L, Castle A. Re-examining the role of hydrogen peroxide in bacteriostatic and bactericidal activities of honey. Front Microbiol 2011; 2: 213.
9. Kwakman PHS, Zaat SAJ. Antibacterial components of honey. IUBMB Life 2012; 64: 48-55.
10. Tumin N, Halim NAA, Shahjahan M, Noor Izani N, Sattar MA, Khan A, et al. Antibacterial activity of local Malaysian honey. Malays J Pharm Sci 2005; 3: 1-10.
11. Zulkhairi Amin FA, Sabri S, Mohammad SM, Ismail M, Chan KW, Ismail N, et al. Therapeutic properties of stingless bee honey in comparison with european bee honey. Adv Pharmacol Sci 2018; 2018: 6179596.
12. Molan PC (2009). Honey: Antimicrobial actions and role in disease management. in: Ahmad I, Aqil F (Eds.), New Strategies Combating Bacterial Infection. Weinheim: Wiley VCH. pp. 229-253.
13. Mandal MD, Mandal S. Honey: its medicinal property and antibacterial activity. Asian Pac J Trop Biomed 2011; 1: 154-160.
14. Zainol MI, Mohd Yusoff K, Mohd Yusof MY. Antibacterial activity of selected Malaysian honey. BMC
Complement Altern Med 2013; 13: 129.
15. Al-kafaween MA, Mohd Hilmi AB, Al-Jamal HAN, Al-Groom RM, Elsahoryi NA, Al-Sayyed H. Potential Antibacterial activity of Yemeni Sidr Honey against Pseudomonas aeruginosa and Streptococcus pyogenes. Anti-Infect Agents 2021; 19: 1-15.
16. Djahmi N, Messad N, Nedjai S, Moussaoui A, Mazouz D, Richard J-L, et al. Molecular epidemiology of Staphylococcus aureus strains isolated from inpatients with infected diabetic foot ulcers in an Algerian University Hospital. Clin Microbiol Infect 2013; 19: E398-404.
17. Al-Kafaween MA, Mohd Hilmi AB, A Nagi Al-Jamal H, A Elsahoryi N, Jaffar N, Khairi Zahri M. Pseudomonas aeruginosa and Streptococcus pyogenes exposed to Malaysian trigona honey in vitro demonstrated downregulation of virulence factor. Iran J Biotechnol 2020; 18(4): e2542.
18. Tarawneh O, Alwahsh W, Abul-Futouh H, Al-Samad LA, Hamadneh L, Abu Mahfouz H, et al. Determination of antimicrobial and antibiofilm activity of combined LVX and AMP impregnated in p (HEMA) Hydrogel. Appl Sci 2021; 11: 8345.
19. 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.
20. 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.
21. Al-kafaween MA, Kafaween H, Al-Groom RM. A comparative study of antibacterial activity of Citrus and Jabali honeys with Manuka honey. Appl Environ Biotechnol 2022; 7: 28-37.
22. Al-Kafaween MA, Hilmi AB, Al-Jamal HA. The beneficial effects of stingless Bee Kelulut honey against Pseudomonas aeruginosa and Streptococcus pyogenes planktonic and biofilm. Trop J Nat Prod Res 2021; 5: 1788-1796.
23. Huwaitat R, Coulter SM, Porter SL, Pentlavalli S, Laverty G. Antibacterial and antibiofilm efficacy of synthetic polymyxin‐mimetic lipopeptides. Pept Sci 2020; 113(1): e24188.
24. 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.
25. 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.
26. Sherlock O, Dolan A, Athman R, Power A, Gethin G, Cowman S, et al. Comparison of the antimicrobial activity of Ulmo honey from Chile and Manuka honey against methicillin-resistant Staphylococcus aureus, Escherichia coli and Pseudomonas aeruginosa. BMC Complement Altern Med 2010; 10: 47.
27. Alkhyat SH, Al-Maqtari M. Effectiveness of antibiotics blended with honey on some pathogenic bacteria species. Int J Microbiol Immunol Res 2014; 2: 109-115.
28. Al-Kafaween MA, Al-Jamal HAN. A comparative study of antibacterial and antivirulence activities of four selected honeys to Manuka honey. Iran J Microbiol 2022; 14: 238-251.
29. 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.
30. Tan HT, Rahman RA, Gan SH, Halim AS, Hassan SA, Sulaiman SA, et al. The antibacterial properties of Malaysian tualang honey against wound and enteric microorganisms in comparison to manuka honey. BMC Complement Altern Med 2009; 9: 34.
31. Singleton P. Bacteria in biology, biotechnology and medicine 6th edition. Wiley 2004. pp1-526.
32. Lu J, Cokcetin NN, Burke CM, Turnbull L, Liu M, Carter DA, et al. Honey can inhibit and eliminate biofilms produced by Pseudomonas aeruginosa. Sci Rep 2019; 9: 18160.
33. Roberts AEL (2014). The inhibition of Pseudomonas aeruginosa by manuka honey.
34. Grecka K, Kuś PM, Worobo RW, Szweda P. Study of the anti-staphylococcal potential of honeys produced in Northern Poland. Molecules 2018; 23: 260.
35. 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.
36. Lu J, Turnbull L, Burke CM, Liu M, Carter DA, Schlothauer RC, et al. Manuka-type honeys can eradicate biofilms produced by Staphylococcus aureus strains with different biofilm-forming abilities. PeerJ 2014; 2: e326.
37. 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.
38. Ahmed AA, Salih FA. Low concentrations of local honey modulate Exotoxin A expression, and quorum sensing related virulence in drug-resistant Pseudomonas aeruginosa recovered from infected burn wounds. Iran J Basic Med Sci 2019; 22: 568-575.
39. Proaño A, Coello D, Villacrés-Granda I, Ballesteros I, Debut A, Vizuete K, et al. 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.
| Files | ||
| Issue | Vol 15 No 1 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i1.11923 | |
| Keywords | ||
| Staphylococcus aureus; Antibacterial; Anti-virulence; Honey; Virulence factors | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Al-Kafaween M, Al-Groom R, Mohd Hilmi AB. Comparison of the antimicrobial and antivirulence activities of Sidr and Tualang honeys with Manuka honey against Staphylococcus aureus. Iran J Microbiol. 2023;15(1):89-101.
