Royal Jelly Aliphatic Acids Contribute to Antimicrobial Activity of Honey

Isidorow, Walerij; Witkowski, Stanisław; Iwaniuk, Piotr; Zambrzycka, Monika; Swiecicka, Izabela

doi:10.2478/jas-2018-0012

Abstract

Honey is valued for its therapeutic qualities which are attributed among others to its antibacterial multifactorial properties. However, all the factors that influence these properties have not been identified. The present study is focused on the antibacterial action of fatty acids originating from royal jelly, the larval food of honeybees. Aliphatic C8-C12 acids characteristic of this bee product had previously been identified in more than fifty different samples of honey originating from seven countries and in eleven samples of Polish herbhoney. Experiments were performed to ascertain the influence of acidity on the antimicrobial activity of the acids. In acidic nutrient media all tested aliphatic hydroxyacids and unsaturated dicarboxylic acids demonstrated antibacterial action against different microbes with minimal inhibitory concentrations between 0.048 and 3.125 mM. Our results confirm that part of the antibacterial activity of honey contributes to these compounds of bee origin.

References

Aljadi, A.M., & Yusoff, K. M. (2003). Isolation and identification of phenolic acids in Malaysian honey with antibacterial properties. Turkish Journal of Medicine, 33, 229-236.
Search in Google Scholar Back to article
Al-Waili, N. S., Salom, K., Butler, G., & Al Ghamdi, A. A. (2011). Honey and microbial infections: A review supporting the use of honey for microbial control. Journal of Medicinal Food, 14, 1079-1096. DOI:10.1089/jmf.2010.016110.1089/jmf.2010.0161
Open DOI Search in Google Scholar Back to article
Barker, S. A., Forster, A. B., Lamb, D. C., & Hodgson, N. (1959). Identification of 10-hydroxy-Δ²-dece-noic acid in royal jelly. Nature, 183, 996-997. DOI: 10.1038/18399a010.1038/183996a0
Search in Google Scholar Back to article
Blum, M. S., Novak, A. F., & Taber, S. (1959). 10-Hydroxy-Δ²-decenoic acid, an antibiotic found in royal jelly. Science, 130, 452-453.10.1126/science.130.3373.452
Search in Google Scholar Back to article
Bogdanov, S. (1997). Nature and origin of the antibacterial substances in honey. Lebensmittel-Wissenschaft und Technologie, 30, 748-753. DOI: 10.1006/fstl.1997.025910.1006/fstl.1997.0259
Open DOI Search in Google Scholar Back to article
Brudzinski, K. (2006). Effect of hydrogen peroxide on antibacterial activity of Canadian honeys. Canadian Journal of Microbiology, 52, 1228-1237.10.1139/w06-086
Search in Google Scholar Back to article
Brudzinski, K., Abubaker, K., St-Martin, L., & Castle., A. (2011). Re-examining the role of hydrogen peroxide in bacteriostatic and bactericidal activities of honey. Frontiers in Microbiology, 2, 213-218. DOI: 10.3389/fmicb.2011.0021310.3389/fmicb.2011.00213
Open DOI Search in Google Scholar Back to article
Brudzinski, K., & Sjaarda, C. (2015). Honey glycoproteins containing antimicrobial peptides, Jelleins of the major royal jelly protein 1, are responsible for the cell wall lytic and bactericidal activities of honey. Plos One 10(4):e0120238. DOI: 10.1371/journal.pone.012023810.1371/journal.pone.0120238
Search in Google Scholar Back to article
Brudzynski, K., Miotto, D., Kim, L., Sjaarda, C., Maldonado-Alvarez, L., Fukś, H. (2017). Active macromolecules of honey form colloidal particles essential for honey antibacterial activity and hydrogen peroxide production. Scientific Reports, 7, 7637. DOI:10.1038/s41598-017-08072-010.1038/s41598-017-08072-0
Open DOI Search in Google Scholar Back to article
Bučeková, M., & Majtán, J. (2016). The MRJP1 honey glycoprotein does not contribute to the overall antibacterial activity of natural honey. European Food Research & Technology, 242, 625-629. DOI: 10.1007/s00217-016-02665-510.1007/s00217-016-02665-5
Open DOI Search in Google Scholar Back to article
Butenant, A., & Rembold, H. (1957). Über den Weiselzellenfuttersaft der Honig Biene. Zeitschrift für Physikalische Chemie, 308, 285-299.10.1515/bchm2.1957.308.1.284
Search in Google Scholar Back to article
Core, E. J., & Schmidt, G. (1979). Useful procedures for the oxidation of alcohols involving pyridinium dichromate in aprotic media. Tetrahedron Letters, 20, 399-402. DOI: 10.1016/S0040-4049(01)93515-410.1016/S0040-4049(01)93515-4
Open DOI Search in Google Scholar Back to article
Fidaleo, M., Zuorro, A., & Lavecchia, R. (2010). Honey: a natural antimicrobial agent against foodborne pathogens? Journal of Biotechnology, 150S, S298. DOI: 10.1016/j.jbiotec.2010.09.25310.1016/j.jbiotec.2010.09.253
Open DOI Search in Google Scholar Back to article
Fyfe, L., Okoro, P., Paterson, U., Coyle, Sh., McDougall, G. J. (2017). Compositional analysis of Scottish honeys with antibacterial activity against antibiotic-resistant bacteria reveals novel antimicrobial components. LWT – Food Science & Technology, 79, 52-59. doi.org/10.1016/j.lwt.2017.01.02310.1016/j.lwt.2017.01.023
Open DOI Search in Google Scholar Back to article
Giles, S. L., & Laheij, R. J. F. (2017). Successful treatment of persistent Clostridium difficile infection with Manuka honey. International Journal of Antimicrobial Agents, 49, 522-523. doi.org/10.1016/j.ijantimicag.2017.02.00510.1016/j.ijantimicag.2017.02.00528257905
Open DOI Search in Google Scholar Back to article
Grecka, K., Kuś, P. M., Worobo, R. W., & Szweda, P. (2018). Study of the anti-staphylococcal potential of honeys produced in Northern Poland. Molecules, 23, 260. DOI:10.3390/molecules2302026010.3390/23020260
Open DOI Search in Google Scholar Back to article
Isidorov, V.A. (2015). Identification of Biologically and Environmentally Significant Organic Compounds. Mass Spectra and Retention Indices Library of Trimethylsilyl Derivatives. PWN, Warszawa. 429 pp.
Search in Google Scholar Back to article
Isidorov, V. A., Czyżewska, U., Isidorova, A. G., & Bakier, S. (2009). Gas chromatographic and mass spectrometric characterization of the organic acids extracted from some preparations containing lyophilized royal jelly. Journal of Chromatography B, 877, 3776-3780. DOI: 10.1016/j.jchromb.2009.09.01610.1016/j.jchromb.2009.09.01619767252
Open DOI Search in Google Scholar Back to article
Isidorov, V. A., Czyżewska, U., Jankowska, E., & Bakier, S. (2011). Determination of royal jelly acids in honey. Food Chemistry, 124, 387-391. DOI: 10.1016/j.food-chem.2010.06.04410.1016/j.food-chem.2010.06.044
Open DOI Search in Google Scholar Back to article
Isidorov, V. A., Bakier, S., & Grzech, J. (2012). Gas chromatographic-mass spectrometric investigation of volatile and extractable compounds of crude royal jelly. Journal of Chromatography B, 885-886, 109-116. DOI: 10.1016/j.jchromb.2011.12.02510.1016/j.jchromb.2011.12.02522245368
Open DOI Search in Google Scholar Back to article
Isidorov, V. A., Bagan, R., Bakier, S., & Swiecicka, I. (2015). Chemical composition and antimicrobial activity of Polish herbhoneys. Food Chemistry, 171, 84-88. DOI: 10.1016/j.foodchem.2014.08.11210.1016/j.foodchem.2014.08.11225308646
Open DOI Search in Google Scholar Back to article
Kwakman, P. H. S., te Velde, A. A., de Boer, L., Vanden-brouke-Grauls, Ch. M. J. E., Zaat, S. A. J. (2010a). Two major medical honeys have different mechanisms of bactericidal activity. PLoS One, 6, e 17709. DOI: 10.1371/journal.pone.001770910.1371/journal.pone.0017709304887621394213
Open DOI Search in Google Scholar Back to article
Kwakman, P. H. S., te Velde, A. A., de Boer, L., Speeijer, D., Vandenbrouke-Grauls, Ch. M. J. E., Zaat, S. A. J. (2010b). How honey kills bacteria. The FASEB Journal, 24, 2567-2582, DOI: 10.1096/fj.09-15078910.1096/fj.09-15078920228250
Open DOI Search in Google Scholar Back to article
Lee, S. K., & Lee, H. (2016). Antibacterial activity of solvent fractions and bacterial isolated of Korean domestic honey from different floral sources. Food Science and Biotechnology, 25, 1507-1512. DOI:10.1007/s10068-016-0234-010.1007/s10068-016-0234-0604926330263438
Open DOI Search in Google Scholar Back to article
Mavric, E., Wittmann, S., Barth, G., & Henle, T. (2008). Identification and quantification of methylglyoxal as the dominant antibacterial constituent of Manuka (Leptospermium scoparium) honeys from New Zealand. Molecular Nutrition & Food Research, 52, 483-489. DOI: 10.1002/mnfr.20070028210.1002/mnfr.200700282
Open DOI Search in Google Scholar Back to article
McCleskey, C. S., & Melampy, R. M. (1938). Bactericidal activity of “Royal Jelly” of honey bees. Journal of Microbiology, 38, 324.
Search in Google Scholar Back to article
Melliou, E., & Chinou, I. (2005). Chemistry and bioactivity of royal jelly from Greece. Agricultural and Food Chemistry, 53, 8987-8992. DOI: 10.1021/jf051550p10.1021/jf051550p
Open DOI Search in Google Scholar Back to article
Mizrahi, H., & Lensky, Y. (Eds.). (1996). Bee products: Properties, applications and apitherapy. NY: Plenum Press.10.1007/978-1-4757-9371-0
Search in Google Scholar Back to article
Moore, O. A., Smith, L. A., Campbell, F., Seers, K., Mc-Quay, H. J., Moore, R. A. (2001). Systematic review of the use of honey as a wound dressing. BMC Complementary & Alternative Medicine, 1, 2-7. http://www.biomedcentral.com/1472-6882/1/210.1186/1472-6882-1-2
Search in Google Scholar Back to article
Russell, K. M., Molan, P. C., Wilkins, A. L., & Holand, P. T. (1988). Identification of some antibacterial constituents of New Zealand Manuka honey. Journal of Agricultural & Food Chemistry, 38, 10-13. DOI: 10.1021/jf00091a00210.1021/jf00091a002
Open DOI Search in Google Scholar Back to article
Skubida, M., Pohorecka, K., Bober, A., & Zdańska, D. (2014). Five-year investigation of Paenibacillus larvae expansion in Polish apiaries: Analyses of results. In: Mat. 51^th Sci. Beekeep. Conf., Szczyrk, pp. 55-56.
Search in Google Scholar Back to article
Sultanbawa, Y., Cozzolino, D., Fuller, S., Cusack, A., Currie, M., Smyth, H. (2015). Infrared spectroscopy as a rapid tool to detect methylglyoxal and antibacterial activity in Australian honeys. Food Chemistry, 172, 207-212. DOI: 10.1016/j.foodchem.2014.09.06710.1016/j.foodchem.2014.09.067
Open DOI Search in Google Scholar Back to article
Tan, S.-T., Holland, P. T., Wilkins, A. L., & Molan, P. C. (1988). Extractivities from New Zealand honeys. White clover, manuka and kanuka unifloral honeys. Journal of Agricultural & Food Chemistry, 36, 453-460. DOI: 10.1021/jf00081a01210.1021/jf00081a012
Open DOI Search in Google Scholar Back to article
Taormina, P. J., Niemira, B. A., & Beuchat, L. R. (2001). Inhibitory activity of honey against foodborne pathogens as influenced by the presence of hydrogen peroxide and level of antioxidant power. International Journal of Food Microbiology, 69, 217-225.10.1016/S0168-1605(01)00505-0
Search in Google Scholar Back to article
Valachová, I., Bučeková, M., & Majtán, J. (2016). Quantification of bee-derived peptide Defensin-1 in honey by competitive enzyme-linked immunosorbent assay, a new approach in honey quality control. Czech Journal of Food Sciences, 34, 233-243. DOI: 10.17221/422/2015-cjfs10.17221/422/2015-CJFS
Search in Google Scholar Back to article
Weston, R. J., Brocklebank, L. K., & Lu, Y. R. (2000). Identification and quantitative levels of antibacterial components of some New Zealand honeys. Food Chemistry, 70, 427-435. DOI: 10.1016/S0308-8146(00)00127-810.1016/S0308-8146(00)00127-8
Open DOI Search in Google Scholar Back to article
Isidorov, V. A., Brzozowska, M., Czyżewska, U., & Glinka, Ł. (2009). Gas chromatographic investigation of phenylpropenoid glycerides from aspen (Populus tremula L.) buds. Journal of Chromatography A, 1198–1199: 196–201. DOI: 10.1016/j.chroma.2008.05.03810.1016/j.chroma.2008.05.03818533164
Open DOI Search in Google Scholar Back to article
Isidorov, V., Szczepaniak, L., & Bakier, S. (2014a). Rapid GC/MS determination of botanical precursors of Eurasian propolis. Food Chemistry, 142, 101–110. DOI: 10.1016/j.foodchem.2013.07.03210.1016/j.foodchem.2013.07.03224001818
Open DOI Search in Google Scholar Back to article
Isidorov, V., Szczepaniak, L., Wróblewska, A., Pirożnikow, E., Vetchinnikova, L. (2014b). Gas chromatographic-mass spectrometric examination of chemical composition of two Eurasian birch (Betula L.) bud exudates and its taxonomical implication. Biochemical Systematics and Ecology, 52, 41–48. DOI: 10.1016/j.bse.2013.12.00810.1016/j.bse.2013.12.008
Open DOI Search in Google Scholar Back to article
Isidorov, V.A. (2015). Identification of Biologically and Environmentally Significant Organic Compounds. Mass Spectra and Retention Indices of Trimethylsilyl Derivatives. PWN, Warsaw, 430 pp.
Search in Google Scholar Back to article
NIST Chemistry WebBook (2013). National Institute of Standards and Technology, Gaithersburg, MD 20899. http://webbook.nist.gov.chemistry.
Search in Google Scholar Back to article

Royal Jelly Aliphatic Acids Contribute to Antimicrobial Activity of Honey

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