1887

Abstract

Many Australian native honeys possess significant antimicrobial properties due to the production of hydrogen peroxide (HO) by glucose oxidase, an enzyme derived from the honeybee. The level of HO produced in different honey samples is highly variable, and factors governing its production and stability are not well understood. In this study, highly active Australian honeys that had been stored for >10 years lost up to 54 % of their antibacterial activity, although almost all retained sufficient activity to be considered potentially therapeutically useful. We used a simple colourimetric assay to quantify HO production. Although we found a significant correlation between HO production and antibacterial activity across diverse honey samples, variation in HO only explained 47 % of the variation observed in activity, limiting the assay as a screening tool and highlighting the complexity of the relationship between HO and the killing power of honey. To further examine this, we tested whether HO detection in honey was being inhibited by pigmented compounds and if HO might be directly degraded in some honey samples. We found no correlation between HO detection and honey colour. Some honey samples rapidly lost endogenous and spiked HO, suggesting that components in honey, such as catalase or antioxidant polyphenols, may degrade or quench HO. Despite this rapid loss of HO, these honeys had significant peroxide-based antibacterial activity, indicating a complex relationship between HO and other honey components that may act synergistically to augment activity.

Funding
This study was supported by the:
  • ElizabethHarry , Agrifutures Australia , (Award PRJ-009186)
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2021-01-28
2021-02-26
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References

  1. Kwakman PHS, Zaat SAJ. Antibacterial components of honey. IUBMB Life 2012; 64: 48 55 [CrossRef]
    [Google Scholar]
  2. Brudzynski K, Miotto D. Honey melanoidins: analysis of the compositions of the high molecular weight melanoidins exhibiting radical-scavenging activity. Food Chem 2011; 127: 1023 1030 [CrossRef] [PubMed]
    [Google Scholar]
  3. Brudzynski K, Miotto D. The relationship between the content of Maillard reaction-like products and bioactivity of Canadian honeys. Food Chem 2011; 124: 869 874 [CrossRef]
    [Google Scholar]
  4. Kwakman PHS, de Boer L, Ruyter-Spira CP, Creemers-Molenaar T, Helsper JPFG et al. Medical-grade honey enriched with antimicrobial peptides has enhanced activity against antibiotic-resistant pathogens. Eur J Clin Microbiol Infect Dis 2011; 30: 251 257 [CrossRef] [PubMed]
    [Google Scholar]
  5. Allen KL, Molan PC, Reid GM. A survey of the antibacterial activity of some New Zealand honeys. J Pharm Pharmacol 1991; 43: 817 822 [CrossRef] [PubMed]
    [Google Scholar]
  6. Brudzynski K, Abubaker K, Wang T. Powerful bacterial killing by buckwheat honeys is concentration-dependent, involves complete DNA degradation and requires hydrogen peroxide. Front Microbiol 2012; 3: 242 [CrossRef] [PubMed]
    [Google Scholar]
  7. White JW, Subers MH, Schepartz AI. The identification of inhibine, the antibacterial factor in honey, as hydrogen peroxide and its origin in a honey glucose-oxidase system. Biochim Biophys Acta 1963; 73: 57 70 [CrossRef]
    [Google Scholar]
  8. Irish J, Blair S, Carter DA. The antibacterial activity of honey derived from Australian flora. PLoS One 2011; 6: e18229 [CrossRef] [PubMed]
    [Google Scholar]
  9. Brady N, Molan P, Bang L. A survey of non-manuka New Zealand honeys for antibacterial and antifungal activities. J Apic Res 2004; 43: 47 52 [CrossRef]
    [Google Scholar]
  10. Chen C, Campbell LT, Blair SE, Carter DA. The effect of standard heat and filtration processing procedures on antimicrobial activity and hydrogen peroxide levels in honey. Front Microbiol 2012; 3: 265 [CrossRef] [PubMed]
    [Google Scholar]
  11. Jonathan W, White JR, Subers MH. Studies on honey inhibine. 4. destruction of the peroxide accumulation system by light. 1964; 29 819 828
  12. Alaux C, Ducloz F, Crauser D, Le Conte Y. Diet effects on honeybee immunocompetence. Biol Lett 2010; 6: 562 565 [CrossRef] [PubMed]
    [Google Scholar]
  13. Weston RJ. The contribution of catalase and other natural products to the antibacterial activity of honey: a review. Food Chem 2000; 71: 235 239 [CrossRef]
    [Google Scholar]
  14. Sroka Z, Cisowski W. Hydrogen peroxide scavenging, antioxidant and anti-radical activity of some phenolic acids. Food Chem Toxicol 2003; 41: 753 758 [CrossRef] [PubMed]
    [Google Scholar]
  15. Irish J, Carter DA, Shokohi T, Blair SE. Honey has an antifungal effect against Candida species. Med Mycol 2006; 44: 289 291 [CrossRef] [PubMed]
    [Google Scholar]
  16. George NM, Cutting KF, Honey A. Antibacterial honey (Medihoney): in-vitro activity against clinical isolates of MRSA, VRE, and other multiresistant gram-negative organisms including Pseudomonas aeruginosa . Wounds 2007; 19: 231 236 [PubMed]
    [Google Scholar]
  17. Carter DA, Blair SE, Cokcetin NN, Bouzo D, Brooks P et al. Therapeutic manuka honey: no longer so alternative. Front Microbiol 2016; 7: 11 [CrossRef]
    [Google Scholar]
  18. Turcotte C, Lacroix C, Kheadr E, Grignon L, Fliss I. A rapid turbidometric microplate bioassay for accurate quantification of lactic acid bacteria bacteriocins. Int J Food Microbiol 2004; 90: 283 293 [CrossRef] [PubMed]
    [Google Scholar]
  19. 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 [CrossRef] [PubMed]
    [Google Scholar]
  20. Lehmann DM, Krishnakumar K, Batres MA, Hakola-Parry A, Cokcetin N et al. A cost-effective colourimetric assay for quantifying hydrogen peroxide in honey. Access Microbiol 2019; 1: e000065 [CrossRef] [PubMed]
    [Google Scholar]
  21. White JW, Beaty MR, Eaton WG, Hart B, Huser W et al. Instrumental color classification of honey: collaborative study. J AOAC Int 1984; 67: 1129 1131 [CrossRef]
    [Google Scholar]
  22. Ferreira ICFR, Aires E, Barreira JCM, Estevinho LM. Antioxidant activity of Portuguese honey samples: different contributions of the entire honey and phenolic extract. Food Chem 2009; 114: 1438 1443 [CrossRef]
    [Google Scholar]
  23. United States standards for grades of extracted honey Agriculture USDo 5 Washington, DC: 1985
    [Google Scholar]
  24. Brudzynski K, Kim L. Storage-induced chemical changes in active components of honey de-regulate its antibacterial activity. Food Chem 2011; 126: 1155 1163 [CrossRef]
    [Google Scholar]
  25. 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 [CrossRef] [PubMed]
    [Google Scholar]
  26. Borutinskaite V, Treigyte G, Ceksteryte V, Kurtinaitiene B, Navakauskiene R. Proteomic identification and enzymatic activity of buckwheat (Fagopyrum esculentum) honey based on different assays. J Food Nutr Res 2018; 57: 57 69
    [Google Scholar]
  27. Schepartz AI. Honey catalase: occurrence and some kinetic properties. J Apic Res 1966; 5: 167 176 [CrossRef]
    [Google Scholar]
  28. Brudzynski K. Effect of hydrogen peroxide on antibacterial activities of Canadian honeys. Can J Microbiol 2006; 52: 1228 1237 [CrossRef] [PubMed]
    [Google Scholar]
  29. Poli JP, Guinoiseau E, Luciani A, Yang Y, Battesti MJ et al. Key role of hydrogen peroxide in antimicrobial activity of spring, honeydew maquis and chestnut grove Corsican honeys on Pseudomonas aeruginosa DNA. Lett Appl Microbiol 2018; 66: 427 433 [CrossRef] [PubMed]
    [Google Scholar]
  30. Anand S, Pang E, Livanos G, Mantri N. Characterization of physico-chemical properties and antioxidant capacities of bioactive honey produced from Australian grown Agastache rugosa and its correlation with colour and poly-phenol content. Molecules 2018; 23: E108 [CrossRef] [PubMed]
    [Google Scholar]
  31. Cokcetin NN, Pappalardo M, Campbell LT, Brooks P, Carter DA et al. The antibacterial activity of Australian Leptospermum honey correlates with methylglyoxal levels. PLoS One 2016; 11: e0167780 [CrossRef] [PubMed]
    [Google Scholar]
  32. Bucekova M, Jardekova L, Juricova V, Bugarova V, Di Marco G et al. Antibacterial activity of different blossom honeys: new findings. Molecules 2019; 24: e1573 [CrossRef] [PubMed]
    [Google Scholar]
  33. Farkasovska J, Bugarova V, Godocikova J, Majtan V, Majtan J. The role of hydrogen peroxide in the antibacterial activity of different floral honeys. Eur Food Res Technol 2019; 245: 2739 2744 [CrossRef]
    [Google Scholar]
  34. Sindi A, Chawn MVB, Hernandez ME, Green K, Islam MK. Anti-Biofilm effects and characterisation of the hydrogen peroxide activity of a range of Western Australian honeys compared to manuka and multifloral honeys. Sci Rep 2019; 9: 17666 [CrossRef] [PubMed]
    [Google Scholar]
  35. Molan PC. The role of honey in the management of wounds. J Wound Care 1999; 8: 415 418 [CrossRef] [PubMed]
    [Google Scholar]
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