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Antibacterial activity of varying UMF-graded Manuka honeys


Autoři: Alodia Girma aff001;  Wonjae Seo aff001;  Rosemary C. She aff001
Působiště autorů: Department of Pathology, Keck School of Medicine of the University of Southern California, Los Angeles, California, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224495

Souhrn

Honey has been used as a traditional remedy for skin and soft tissue infections due to its ability to promote wound healing. Manuka honey is recognized for its unusually abundant content of the antibacterial compound, methylglyoxal (MGO). The Unique Manuka Factor (UMF) grading system reflects the MGO concentration in Manuka honey sold commercially. Our objective was to observe if UMF values correlated with the antibacterial activity of Manuka honey against a variety of pathogens purchased over the counter. The antibacterial effect of Manuka honey with UMF values of 5+, 10+, and 15+ from the same manufacturer was assessed by the broth microdilution method. Minimum inhibitory concentration (MIC) values were determined against 128 isolates from wound cultures representing gram-positive, gram-negative, drug-susceptible, and multi-drug resistant (MDR) organisms. Lower MICs were observed with UMF 5+ honey for staphylococci (n = 73, including 25 methicillin-resistant S. aureus) and Pseudomonas aeruginosa (n = 22, including 10 MDR) compared to UMF 10+ honey (p<0.05) and with UMF 10+ compared to UMF 15+ (p = 0.01). For Enterobacteriaceae (n = 33, including 14 MDR), MIC values were significantly lower for UMF 5+ or UMF 10+ compared to UMF 15+ honey (p<0.01). MIC50 for UMF 5+, UMF 10+, and UMF 15+ honey against staphylococci was 6%, 7%, and 15%, and for Enterobacteriaceae was 21%, 21%, and 27%, respectively. For Pseudomonas aeruginosa MIC50 was 21% and MIC90 was 21–27% for all UMFs. Manuka honey exhibited antimicrobial activity against a spectrum of organisms including those with multi-drug resistance, with more potent activity overall against gram-positive than gram-negative bacteria. Manuka honey with lower UMF values, in our limited sampling, paradoxically demonstrated increased antimicrobial activity among the limited samples tested, presumably due to changes in MGO content of honey over time. The UMF value by itself may not be a reliable indicator of antibacterial effect.

Klíčová slova:

Antibacterials – Antimicrobials – Enterobacteriaceae – Gram negative bacteria – Methicillin-resistant Staphylococcus aureus – Pseudomonas aeruginosa – Staphylococcus – Honey


Zdroje

1. Oryan A, Alemzadeh E, Moshiri A. Biological properties and therapeutic activities of honey in wound healing: A narrative review and meta-analysis. J Tissue Viability. 2016;25(2):98–118. doi: 10.1016/j.jtv.2015.12.002 26852154

2. Eteraf-Oskouei T, Najafi M. Traditional and modern uses of natural honey in human diseases: a review. Iran J Basic Med Sci. 2013;16(6):731–42. 23997898

3. Carter DA, Blair SE, Cokcetin NN, Bouzo D, Brooks P, Schothauer R, et al. Therapeutic Manuka Honey: No Longer So Alternative. Front Microbiol. 2016;7:569. doi: 10.3389/fmicb.2016.00569 27148246

4. Salonen A, Virjamo V, Tammela P, Fauch L, Julkunen-Tiitto R. Screening bioactivity and bioactive constituents of Nordic unifloral honeys. Food Chem. 2017;237:214–224. doi: 10.1016/j.foodchem.2017.05.085 28763988 Epub May 18.

5. Alvarez-Suarez JM, Gasparrini M, Forbes-Hernandez TY, Mazzoni L, Giampieri F. The Composition and Biological Activity of Honey: A Focus on Manuka Honey. Foods. 2014;3(3):420–32. doi: 10.3390/foods3030420 28234328

6. Blair SE, Cokcetin NN, Harry EJ, Carter DA. The unusual antibacterial activity of medical-grade Leptospermum honey: antibacterial spectrum, resistance and transcriptome analysis. Eur J Clin Microbiol Infect Dis. 2009;28(10):1199–208. doi: 10.1007/s10096-009-0763-z 19513768

7. Jenkins R, Burton N, Cooper R. Manuka honey inhibits cell division in methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother. 2011;66(11):2536–42. doi: 10.1093/jac/dkr340 21903658

8. 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(2):167–71. doi: 10.1007/s10096-010-1065-1 20936493

9. 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(4):483–9. doi: 10.1002/mnfr.200700282 18210383

10. Cokcetin NN, Pappalardo M, Campbell LT, Brooks P, Carter DA, Blair SE, et al. The Antibacterial Activity of Australian Leptospermum Honey Correlates with Methylglyoxal Levels. PLoS One. 2016;11(12):e0167780. doi: 10.1371/journal.pone.0167780 28030589

11. Almasaudi SB, Al-Nahari AAM, Abd El-Ghany ESM, Barbour E, Al Muhayawi SM, Al-Jaouni S, et al. Antimicrobial effect of different types of honey on. Saudi J Biol Sci. 2017;24(6):1255–61. doi: 10.1016/j.sjbs.2016.08.007 28855819

12. Molan P. An explanation of why the MGO level in manuka honey does not show the antibacterial activity. New Zealand BeeKeeper. 2008;16:11–3.

13. Kwakman PH, Te Velde AA, de Boer L, Vandenbroucke-Grauls CM, Zaat SA. Two major medicinal honeys have different mechanisms of bactericidal activity. PLoS One. 2011;6(3):e17709. doi: 10.1371/journal.pone.0017709 21394213

14. Allen KL, Molan PC, Reid GM. A survey of the antibacterial activity of some New Zealand honeys. J Pharm Pharmacol. 1991;43(12):817–22. doi: 10.1111/j.2042-7158.1991.tb03186.x 1687577

15. Unique Manuka Factor Honey Association. Grading System Explained. 2019 [cited 14 August 2019]. In: UMF Honey Association Website [Internet]. St. Heliers, New Zealand. https://www.umf.org.nz/grading-system-explained/.

16. CLSI. Methods for Dilution Antimicrobial Susceptibilities Tests for Bacteria that Grow Aerobically; Approved Standard, 11th edition. CLSI document M07-A10. Wayne, PA: Clinical Laboratory and Standards Institute; 2018.

17. CDC. Antimicrobial Resistant Phenotype Definitions. 2016; https://www.cdc.gov/nhsn/pdfs/ps-analysis-resources/phenotype_definitions.pdf

18. Hawkey PM. Multidrug-resistant Gram-negative bacteria: a product of globalization. J Hosp Infect. 2015;89(4):241–7. doi: 10.1016/j.jhin.2015.01.008 25737092

19. Combarros-Fuertes P, Estevinho LM, Teixeira-Santos R, Rodrigues AG, Pina-Vaz C, Fresno JM, et al. Evaluation of Physiological Effects Induced by Manuka Honey Upon Staphylococcus aureus and Escherichia coli. Microorganisms. 2019;7(8).(pii):microorganisms7080258.

20. Liu M, Lu J, Müller P, Turnbull L, Burke CM, Schlothauer RC, et al. Antibiotic-specific differences in the response of Staphylococcus aureus to treatment with antimicrobials combined with manuka honey. Front Microbiol. 2014;5:779. doi: 10.3389/fmicb.2014.00779 25674077

21. Jenkins RE, Cooper R. Synergy between oxacillin and manuka honey sensitizes methicillin-resistant Staphylococcus aureus to oxacillin. J Antimicrob Chemother. 2012;67(6):1405–7. doi: 10.1093/jac/dks071 22382468

22. Piotrowski M, Karpinski P, Pituch H, van Belkum A, Obuch-Woszczatynski P. Antimicrobial effects of Manuka honey on in vitro biofilm formation by Clostridium difficile. Eur J Clin Microbiol Infect Dis. 2017;36(9):1661–4. doi: 10.1007/s10096-017-2980-1 28417271 Epub 2017 Apr 18.

23. Lee VS, Humphreys IM, Purcell PL, Davis GE. Manuka honey sinus irrigation for the treatment of chronic rhinosinusitis: a randomized controlled trial. Int Forum Allergy Rhinol. 2017;7(4):365–72. doi: 10.1002/alr.21898 27935259

24. Kamaratos AV, Tzirogiannis KN, Iraklianou SA, Panoutsopoulos GI, Kanellos IE, Melidonis AI. Manuka honey-impregnated dressings in the treatment of neuropathic diabetic foot ulcers. Int Wound J. 2014;11(3):259–63. doi: 10.1111/j.1742-481X.2012.01082.x 22985336

25. Alangari AA, Morris K, Lwaleed BA, Lau L, Jones K, Cooper R, et al. Honey is potentially effective in the treatment of atopic dermatitis: Clinical and mechanistic studies. Immun Inflamm Dis. 2017;5(2):190–9. doi: 10.1002/iid3.153 28474502

26. Malhotra R, Ziahosseini K, Poitelea C, Litwin A, Sagili S. Effect of Manuka Honey on Eyelid Wound Healing: A Randomized Controlled Trial. Ophthalmic Plast Reconstr Surg. 2017;33(4):268–72. doi: 10.1097/IOP.0000000000000743 27429228

27. Roberts AEL, Powell LC, Pritchard MF, Thomas DW, Jenkins RE. Anti-pseudomonad Activity of Manuka Honey and Antibiotics in a Specialized. Front Microbiol. 2019;10:869. doi: 10.3389/fmicb.2019.00869 31105667

28. Jenkins R, Wootton M, Howe R, Cooper R. Susceptibility to manuka honey of Staphylococcus aureus with varying sensitivities to vancomycin. Int J Antimicrob Agents. 2012;40(1):88–9. doi: 10.1016/j.ijantimicag.2012.03.014 22580029

29. French VM, Cooper RA, Molan PC. The antibacterial activity of honey against coagulase-negative staphylococci. J Antimicrob Chemother. 2005;56(1):228–31. doi: 10.1093/jac/dki193 15941774

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. doi: 10.1186/1472-6882-9-34 19754926

31. Hixon KR, Lu T, McBride-Gagyi SH, Janowiak BE, Sell SA. A Comparison of Tissue Engineering Scaffolds Incorporated with Manuka Honey of Varying UMF. Biomed Res Int. 2017;2017:4843065. doi: 10.1155/2017/4843065 28326322

32. Al-Nahari AA, Almasaudi SB, Abd El-Ghany eS, Barbour E, Al Jaouni SK, Harakeh S. Antimicrobial activities of Saudi honey against Pseudomonas aeruginosa. Saudi J Biol Sci. 2015;22(5):521–5. doi: 10.1016/j.sjbs.2015.04.006 26288553

33. Atrott J, Haberlau S, Henle T. Studies on the formation of methylglyoxal from dihydroxyacetone in Manuka (Leptospermum scoparium) honey. Carbohydr Res. 2012;361:7–11. doi: 10.1016/j.carres.2012.07.025 22960208

34. Grainger MN, Manley-Harris M, Lane JR, Field RJ. Kinetics of conversion of dihydroxyacetone to methylglyoxal in New Zealand mānuka honey: Part I—Honey systems. Food Chem. 2016;202:484–91. doi: 10.1016/j.foodchem.2016.02.029 26920322

35. Jaine J. Test results for packed Manuka honey. New Zealand Beekeeper. 2018;26:16–7.


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