Antibacterial properties of selected Malaysian Tualang honey against Pseudomonas aeruginosa and Streptococcus pyogenes
-
Mohammad Abdulraheem Al-Kafaween
,
Hamid Ali Nagi Al-Jamal
,
Abu Bakar Mohd Hilmi
,
Nour Amin Elsahoryi
,
Norzawani Jaffar
,
Mohd Khairi Zahri
Abstract
Background and Objectives: Tualang honey (TH) is a Malaysian multifloral jungle honey. In recent years, there has been a marked increase in the number of studies published in medical databases regarding its potential health benefits. The study aimed to investigate the effect of TH against Pseudomonas aeruginosa and Streptococcus pyogenes.
Materials and Methods: The effect of TH on both bacteria was investigated using MIC, MBC, growth curve, time-kill curve, scanning electron microscopy (SEM) and RT-qPCR.
Results: The MIC of TH against P. aeruginosa and S. pyogenes was 18.5% (w/v) and 13% (w/v) respectively and MBC was 25% (w/v) for both bacteria. Spectrophotometric readings of at least 90% inhibition yielded MIC90 values of TH, 18.5% (w/v) and 15% (w/v) for P. aeruginosa and S. pyogenes respectively. A time–kill curve demonstrated a bactericidal with a 4-log reduction estimated within 8 hours. Using SEM, loss of structural integrity and marked changes in cell shape were observed. RT-qPCR analysis showed that TH reduced the pattern of gene expression in both bacteria, with a trend toward reduced expression of the virulence genes of interest.
Conclusion: This study suggests that TH could potentially be used as an alternative therapeutic agent for microbial infection particularly against these two organisms.
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14. Abbas HA. Comparative antibacterial and antibiofilm activities of manuka honey and Egyptian clover honey. Asian J Appl Sci 2014;2:110-115.
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17. 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.
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25. 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.
26. Kustiawan PM, Puthong S, Arung ET, Chanchao C. In vitro cytotoxicity of Indonesian stingless bee products against human cancer cell lines. Asian Pac J Trop Biomed 2014;4:549-556.
27. Tan HT, Rahman RA, Gan SH, Halim AS, Asma'Hassan S, 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.
28. Irish J, Blair S, Carter DA. The antibacterial activity of honey derived from Australian flora. PLoS One 2011; 6(3):e18229.
29. Biluca FC, Braghini F, Gonzaga LV, Costa ACO, Fett R. Physicochemical profiles, minerals and bioactive compounds of stingless bee honey (Meliponinae). J Food Compost Anal 2016;50:61-69.
30. Al-Hatamleh MA, Boer JC, Wilson KL, Plebanski M, Mohamud R, Mustafa MZ. Antioxidant-based medicinal properties of stingless bee products: recent progress and future directions. Biomolecules 2020;10:923.
31. Al-Kafaween MA, Hilmi ABM, Khan RS, Bouacha M, Amonov M. Effect of Trigona honey on Escherichia coli cell culture growth: In vitro study. J Apither 2019;5:10-17.
32. Al-kafaween MA, Hilmi ABM, Jaffar N, Al-Jamal HAN, Zahri MK, Amonov M, et al. Effects of Trigona honey on the gene expression profile of Pseudomonas aeruginosa ATCC 10145 and Streptococcus pyogenes ATCC 19615. Jordan J Biol Sci 2020;13: 133-138.
33. Al-kafaween MA, Hilmi ABM, Jaffar N, Al-Jamal HAN, Zahri MK, Jibril FI. Antibacterial and antibiofilm activities of Malaysian Trigona honey against Pseudomonas aeruginosa ATCC 10145 and Streptococcus pyogenes ATCC 19615. Jordan J Biol Sci 2020;13:69-76.
34. Zainol MI, Yusoff KM, Yusof MYM. Antibacterial activity of selected Malaysian honey. BMC Complement Altern Med 2013;13:129.
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. Henriques A, Jenkins R, Burton N, Cooper R. The effect of manuka honey on the structure of Pseudomonas aeruginosa. Eur J Clin Microbiol Infect Dis 2011;30:167-171.
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. Roberts AEL (2014). The inhibition of Pseudomonas aeruginosa by manuka honey: Cardiff Metropolitan University Thesis.
39. Zumla A, Lulat A (1989). Honey-a remedy rediscovered. SAGE Publications Sage UK: London England.
40. Okeke MI, Iroegbu CU, Eze E, Okoli A, Esimone C. Evaluation of extracts of the root of Landolphia owerrience for antibacterial activity. J Ethnopharmacol 2001;78:119-127.
41. Patton T, Barrett J, Brennan J, Moran N. Use of a spectrophotometric bioassay for determination of microbial sensitivity to manuka honey. J Microbiol Methods 2006;64:84-95.
42. Shrivastava SM, Kumar S, Chaudhary M. Time-kill curve studies of Ampucare against Escherichia coli, Staphylococcus aureus, Klebsiella pneumoniae and Proteus vulgaris. Res J Med Plant 2009; 3:116-122.
43. Bucekova M, Buriova M, Pekarik L, Majtan V, Majtan J. Phytochemicals-mediated production of hydrogen peroxide is crucial for high antibacterial activity of honeydew honey. Sci Rep 2018; 8:9061.
2. Majtán J. [Apitherapy--the role of honey in the chronic wound healing process]. Epidemiol Mikrobiol Imunol 2009; 58:137-140.
3. Vandamme L, Heyneman A, Hoeksema H, Verbelen J, Monstrey S. Honey in modern wound care: a systematic review. Burns 2013;39:1514-1525.
4. Lotfy M, Badra G, Burham W, Alenzi F. Combined use of honey, bee propolis and myrrh in healing a deep, infected wound in a patient with diabetes mellitus. Br J Biomed Sci 2006;63:171-173.
5. Subrahmanyam M. A prospective randomised clinical and histological study of superficial burn wound healing with honey and silver sulfadiazine. Burns 1998;24:157-161.
6. Kumar A, Cascarini L, McCaul JA, Kerawala CJ, Coombes D, Godden D, et al. How should we manage oral leukoplakia. Br J Oral Maxillofac Surg 2013;51:377-383.
7. Lusby PE, Coombes AL, Wilkinson JM. Bactericidal activity of different honeys against pathogenic bacteria. Arch Med Res 2005;36:464-477.
8. Molan PC. The antibacterial activity of honey: 1. The nature of the antibacterial activity. Bee World 1992;73:5-28.
9. Mundo MA, Padilla-Zakour OI, Worobo RW. Growth inhibition of foodborne pathogens and food spoilage organisms by select raw honeys. Int J Food Microbiol 2004;97:1-8.
10. Brudzynski K, Abubaker K, Castle A. Re-examining the role of hydrogen peroxide in bacteriostatic and bactericidal activities of honey. Front Microbiol 2011;2:213.
11. 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.
12. Revello MG, Gorini G, Zavattoni M, Furione M, Gerna G. Congenital rubella infection following rubella outbreak in northern Italy, 2002: need for an effective vaccination programme. Eur J Clin Microbiol Infect Dis 2004;23:780-783.
13. 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.
14. Abbas HA. Comparative antibacterial and antibiofilm activities of manuka honey and Egyptian clover honey. Asian J Appl Sci 2014;2:110-115.
15. Roberts AE, 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.
16. Wang R, Starkey M, Hazan R, Rahme L. Honey’s ability to counter bacterial infections arises from both bactericidal compounds and QS inhibition. Front Microbiol 2012;3:144.
17. 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.
18. 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.
19. 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 Pac J Trop Dis 2014;4:194-200.
20. 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.
21. Lu J, Carter DA, Turnbull L, Rosendale D, Hedderley D, Stephens J, et al. The effect of New Zealand kanuka, manuka and clover honeys on bacterial growth dynamics and cellular morphology varies according to the species. PLoS One 2013;8(2):e55898.
22. 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.
23. Ng W, Ken K-W, Kumar R-V, Gunasagaran H, Chandramogan V, Lee Y-Y. 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.
24. Boorn K, Khor YY, Sweetman E, Tan F, Heard T, Hammer K. 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.
25. 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.
26. Kustiawan PM, Puthong S, Arung ET, Chanchao C. In vitro cytotoxicity of Indonesian stingless bee products against human cancer cell lines. Asian Pac J Trop Biomed 2014;4:549-556.
27. Tan HT, Rahman RA, Gan SH, Halim AS, Asma'Hassan S, 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.
28. Irish J, Blair S, Carter DA. The antibacterial activity of honey derived from Australian flora. PLoS One 2011; 6(3):e18229.
29. Biluca FC, Braghini F, Gonzaga LV, Costa ACO, Fett R. Physicochemical profiles, minerals and bioactive compounds of stingless bee honey (Meliponinae). J Food Compost Anal 2016;50:61-69.
30. Al-Hatamleh MA, Boer JC, Wilson KL, Plebanski M, Mohamud R, Mustafa MZ. Antioxidant-based medicinal properties of stingless bee products: recent progress and future directions. Biomolecules 2020;10:923.
31. Al-Kafaween MA, Hilmi ABM, Khan RS, Bouacha M, Amonov M. Effect of Trigona honey on Escherichia coli cell culture growth: In vitro study. J Apither 2019;5:10-17.
32. Al-kafaween MA, Hilmi ABM, Jaffar N, Al-Jamal HAN, Zahri MK, Amonov M, et al. Effects of Trigona honey on the gene expression profile of Pseudomonas aeruginosa ATCC 10145 and Streptococcus pyogenes ATCC 19615. Jordan J Biol Sci 2020;13: 133-138.
33. Al-kafaween MA, Hilmi ABM, Jaffar N, Al-Jamal HAN, Zahri MK, Jibril FI. Antibacterial and antibiofilm activities of Malaysian Trigona honey against Pseudomonas aeruginosa ATCC 10145 and Streptococcus pyogenes ATCC 19615. Jordan J Biol Sci 2020;13:69-76.
34. Zainol MI, Yusoff KM, Yusof MYM. Antibacterial activity of selected Malaysian honey. BMC Complement Altern Med 2013;13:129.
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. Henriques A, Jenkins R, Burton N, Cooper R. The effect of manuka honey on the structure of Pseudomonas aeruginosa. Eur J Clin Microbiol Infect Dis 2011;30:167-171.
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. Roberts AEL (2014). The inhibition of Pseudomonas aeruginosa by manuka honey: Cardiff Metropolitan University Thesis.
39. Zumla A, Lulat A (1989). Honey-a remedy rediscovered. SAGE Publications Sage UK: London England.
40. Okeke MI, Iroegbu CU, Eze E, Okoli A, Esimone C. Evaluation of extracts of the root of Landolphia owerrience for antibacterial activity. J Ethnopharmacol 2001;78:119-127.
41. Patton T, Barrett J, Brennan J, Moran N. Use of a spectrophotometric bioassay for determination of microbial sensitivity to manuka honey. J Microbiol Methods 2006;64:84-95.
42. Shrivastava SM, Kumar S, Chaudhary M. Time-kill curve studies of Ampucare against Escherichia coli, Staphylococcus aureus, Klebsiella pneumoniae and Proteus vulgaris. Res J Med Plant 2009; 3:116-122.
43. Bucekova M, Buriova M, Pekarik L, Majtan V, Majtan J. Phytochemicals-mediated production of hydrogen peroxide is crucial for high antibacterial activity of honeydew honey. Sci Rep 2018; 8:9061.
| Files | ||
| Issue | Vol 12 No 6 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i6.5031 | |
| Keywords | ||
| Antibacterial activity; Tulang honey; Scanning electron microscopy; Differential expression | ||
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How to Cite
1.
Al-Kafaween M, Al-Jamal H, Mohd Hilmi AB, Elsahoryi N, Jaffar N, Zahri M. Antibacterial properties of selected Malaysian Tualang honey against Pseudomonas aeruginosa and Streptococcus pyogenes. Iran J Microbiol. 2020;12(6):565-576.
