Czech Honeydew Honeys-A Potential Source of Local Medical Honey with Strong Antimicrobial Activity
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
SV/FVZ202009
The Specific University Research provided by Ministry of Education Youth and Sports
DZRO-FVZ22-ZHN II
The Ministry of Defence of the Czech Republic
PubMed
39065691
PubMed Central
PMC11279865
DOI
10.3390/ph17070840
PII: ph17070840
Knihovny.cz E-resources
- Keywords
- antibacterial effect, honeydew, hydrogen peroxide, polyphenolic compounds,
- Publication type
- Journal Article MeSH
An increasing resistance of microbes to antibiotics, the emergence of multidrug-resistant and extremely resistant strains, and the long time needed to develop new antibiotics are driving the search for additional sources of antibacterial agents. The aim of the study was to compare the efficacy of Czech honeys with already available pharmaceutical agents containing medicinal honey, and to perform basic biochemical analysis of Czech samples, including detection of undesirable chemical substances. The results showed strong antibacterial activity of Czech honeydew honeys compared to the control group, especially against G+ pathogens, with an average MIC of 9.44% compared to 17.54%, and comparable activity against G- of 16.48% versus 16.66%. In addition to the strong antibacterial activity, this study confirmed the safety and quality of Czech honeys and helped to select the character of a possible source for in vivo testing and subsequent clinical trials.
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van Middendorp J.J., Sanchez G.M., Burridge A.L. The Edwin Smith Papyrus: A Clinical Reappraisal of the Oldest Known Document on Spinal Injuries. Eur. Spine J. 2010;19:1815–1823. doi: 10.1007/s00586-010-1523-6. PubMed DOI PMC
Dustmann J.H. Antibacterial Effect of Honey. Apiacta. 1979;14:7–11.
Bucekova M., Jardekova L., Juricova V., Bugarova V., Di Marco G., Gismondi A., Leonardi D., Farkasovska J., Godocikova J., Laho M., et al. Antibacterial Activity of Different Blossom Honeys: New Findings. Molecules. 2019;24:1573. doi: 10.3390/molecules24081573. PubMed DOI PMC
El Sohaimy S.A., Masry S.H.D., Shehata M.G. Physicochemical Characteristics of Honey from Different Origins. Ann. Agric. Sci. 2015;60:279–287. doi: 10.1016/j.aoas.2015.10.015. DOI
Bischofberger A.M., Pfrunder Cardozo K.R., Baumgartner M., Hall A.R. Evolution of Honey Resistance in Experimental Populations of Bacteria Depends on the Type of Honey and Has No Major Side Effects for Antibiotic Susceptibility. Evol. Appl. 2021;14:1314–1327. doi: 10.1111/eva.13200. PubMed DOI PMC
Troller J., Christian J.H.B. Water Activity and Food. Elsevier Science; Amsterdam, The Netherlands: 1978.
Chirife J., Zamora M., Motto A. The Correlation between Water Activity and % Moisture in Honey: Fundamental Aspects and Application to Argentine Honeys. J. Food Eng. 2006;72:287–292. doi: 10.1016/j.jfoodeng.2004.12.009. DOI
Beckh G., Wessel P., Lüllmann C. Natürliche Bestandteile des Honigs: Hefen und deren Stoffwechselprodukte–Teil 2: Der Wassergehalt und die Wasseraktivität als Qualitätsparameter mit Bezug zum Hefewachstum. Dtsch. Lebensm. -Rundsch. 2004;100:14–17.
The Water Activity of Honey and Related Sugar Solutions. [(accessed on 20 April 2024)]. Available online: https://ira.agroscope.ch/en-US/Page/Publikation?einzelpublikationId=12356&parentUrl=%2Fde-CH%2FPage%2FPublikationsliste%3Fguid%3D85894ecf-e9e1-4c3f-8499-314daea7244c%26page%3D1693.
Cianciosi D., Forbes-Hernández T.Y., Afrin S., Gasparrini M., Reboredo-Rodriguez P., Manna P.P., Zhang J., Bravo Lamas L., Martínez Flórez S., Agudo Toyos P., et al. Phenolic Compounds in Honey and Their Associated Health Benefits: A Review. Molecules. 2018;23:2322. doi: 10.3390/molecules23092322. PubMed DOI PMC
Sherlock O., Dolan A., Athman R., Power A., Gethin G., Cowman S., Humphreys H. 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. doi: 10.1186/1472-6882-10-47. PubMed DOI PMC
Vasić V., Đurđić S., Tosti T., Radoičić A., Lušić D., Milojković-Opsenica D., Tešić Ž., Trifković J. Two Aspects of Honeydew Honey Authenticity: Application of Advance Analytical Methods and Chemometrics. Food Chem. 2020;305:125457. doi: 10.1016/j.foodchem.2019.125457. PubMed DOI
Lachman J., Orsák M., Hejtmánková A., Kovářová E. Evaluation of Antioxidant Activity and Total Phenolics of Selected Czech Honeys. LWT—Food Sci. Technol. 2010;43:52–58. doi: 10.1016/j.lwt.2009.06.008. DOI
Alaerjani W.M.A., Abu-Melha S., Alshareef R.M.H., Al-Farhan B.S., Ghramh H.A., Al-Shehri B.M.A., Bajaber M.A., Khan K.A., Alrooqi M.M., Modawe G.A., et al. Biochemical Reactions and Their Biological Contributions in Honey. Molecules. 2022;27:4719. doi: 10.3390/molecules27154719. PubMed DOI PMC
Brudzynski K. A Current Perspective on Hydrogen Peroxide Production in Honey. A Review. Food Chem. 2020;332:127229. doi: 10.1016/j.foodchem.2020.127229. PubMed DOI
Grzesik M., Bartosz G., Stefaniuk I., Pichla M., Namieśnik J., Sadowska-Bartosz I. Dietary Antioxidants as a Source of Hydrogen Peroxide. Food Chem. 2019;278:692–699. doi: 10.1016/j.foodchem.2018.11.109. PubMed DOI
Da Silva P.M., Gauche C., Gonzaga L.V., Costa A.C.O., Fett R. Honey: Chemical Composition, Stability and Authenticity. Food Chem. 2016;196:309–323. doi: 10.1016/j.foodchem.2015.09.051. PubMed DOI
Endo A., Salminen S. Honeybees and Beehives Are Rich Sources for Fructophilic Lactic Acid Bacteria. Syst. Appl. Microbiol. 2013;36:444–448. doi: 10.1016/j.syapm.2013.06.002. PubMed DOI
Carter C., Thornburg R.W. Tobacco Nectarin I. Purification and Characterization as a Germin-like, Manganese Superoxide Dismutase Implicated in the defensE of Floral Reproductive Tissues. J. Biol. Chem. 2000;275:36726–36733. doi: 10.1074/jbc.M006461200. PubMed DOI
Carter C.J., Thornburg R.W. Tobacco Nectarin V Is a Flavin-Containing Berberine Bridge Enzyme-like Protein with Glucose Oxidase Activity. Plant Physiol. 2004;134:460–469. doi: 10.1104/pp.103.027482. PubMed DOI PMC
Brudzynski K. Unexpected Value of Honey Color for Prediction of a Non-Enzymatic H2O2 Production and Honey Antibacterial Activity: A Perspective. Metabolites. 2023;13:526. doi: 10.3390/metabo13040526. PubMed DOI PMC
Almasaudi S. The Antibacterial Activities of Honey. Saudi J. Biol. Sci. 2021;28:2188–2196. doi: 10.1016/j.sjbs.2020.10.017. PubMed DOI PMC
McLoone P., Warnock M., Fyfe L. Honey: A Realistic Antimicrobial for Disorders of the Skin. J. Microbiol. Immunol. Infect. 2016;49:161–167. doi: 10.1016/j.jmii.2015.01.009. PubMed DOI
Tseng J.-M., Huang J.-R., Huang H.-C., Tzen J.T.C., Chou W.-M., Peng C.-C. Facilitative Production of an Antimicrobial Peptide Royalisin and Its Antibody via an Artificial Oil-Body System. Biotechnol. Prog. 2011;27:153–161. doi: 10.1002/btpr.528. PubMed DOI
Bucekova M., Sojka M., Valachova I., Martinotti S., Ranzato E., Szep Z., Majtan V., Klaudiny J., Majtan J. Bee-Derived Antibacterial Peptide, Defensin-1, Promotes Wound Re-Epithelialisation in Vitro and in Vivo. Sci. Rep. 2017;7:7340. doi: 10.1038/s41598-017-07494-0. PubMed DOI PMC
Nolan V.C., Harrison J., Cox J.A.G. Dissecting the Antimicrobial Composition of Honey. Antibiotics. 2019;8:251. doi: 10.3390/antibiotics8040251. PubMed DOI PMC
Grainger M.N.C., Manley-Harris M., Lane J.R., Field R.J. Kinetics of the Conversion of Dihydroxyacetone to Methylglyoxal in New Zealand Mānuka Honey: Part II--Model Systems. Food Chem. 2016;202:492–499. doi: 10.1016/j.foodchem.2016.02.030. PubMed DOI
Majtan J., Klaudiny J., Bohova J., Kohutova L., Dzurova M., Sediva M., Bartosova M., Majtan V. Methylglyoxal-Induced Modifications of Significant Honeybee Proteinous Components in Manuka Honey: Possible Therapeutic Implications. Fitoterapia. 2012;83:671–677. doi: 10.1016/j.fitote.2012.02.002. PubMed DOI
Adams C.J., Manley-Harris M., Molan P.C. The Origin of Methylglyoxal in New Zealand Manuka (Leptospermum scoparium) Honey. Carbohydr. Res. 2009;344:1050–1053. doi: 10.1016/j.carres.2009.03.020. PubMed DOI
Roberts A.E.L., Brown H.L., Jenkins R.E. On the Antibacterial Effects of Manuka Honey: Mechanistic Insights. RRB. 2015;6:215–224. doi: 10.2147/RRB.S75754. DOI
Arena E., Ballistreri G., Tomaselli F., Fallico B. Survey of 1,2-Dicarbonyl Compounds in Commercial Honey of Different Floral Origin. J. Food Sci. 2011;76:C1203–C1210. doi: 10.1111/j.1750-3841.2011.02352.x. PubMed DOI
Degen J., Hellwig M., Henle T. 1,2-Dicarbonyl Compounds in Commonly Consumed Foods. J. Agric. Food Chem. 2012;60:7071–7079. doi: 10.1021/jf301306g. PubMed DOI
Laallam H., Boughediri L., Bissati S., Menasria T., Mouzaoui M.S., Hadjadj S., Hammoudi R., Chenchouni H. Modeling the Synergistic Antibacterial Effects of Honey Characteristics of Different Botanical Origins from the Sahara Desert of Algeria. Front. Microbiol. 2015;6:01239. doi: 10.3389/fmicb.2015.01239. PubMed DOI PMC
Hermanns R., Mateescu C., Thrasyvoulou A., Tananaki C., Wagener F.A.D.T.G., Cremers N.A.J. Defining the Standards for Medical Grade Honey. J. Apic. Res. 2020;59:125–135. doi: 10.1080/00218839.2019.1693713. DOI
Dzugan M., Ciszkowicz E., Tomczyk M., Miłek M., Lecka-Szlachta K. Coniferous Honeydew Honey: Antibacterial Activity and Anti-Migration Properties against Breast Cancer Cell Line (MCF-7) Appl. Sci. 2024;14:710. doi: 10.3390/app14020710. DOI
Kocyigit A., Aydogdu G., Balkan E., Yenigun V.B., Guler E.M., Bulut H., Koktasoglu F., Gören A.C., Atayoglu A.T. Quercus Pyrenaica Honeydew Honey With High Phenolic Contents Cause DNA Damage, Apoptosis, and Cell Death Through Generation of Reactive Oxygen Species in Gastric Adenocarcinoma Cells. Integr. Cancer Ther. 2019;18:1534735419876334. doi: 10.1177/1534735419876334. PubMed DOI PMC
Zulkifli N.A., Hassan Z., Mustafa M.Z., Azman W.N.W., Hadie S.N.H., Ghani N., Mat Zin A.A. The Potential Neuroprotective Effects of Stingless Bee Honey. Front. Aging Neurosci. 2023;14:1048028. doi: 10.3389/fnagi.2022.1048028. PubMed DOI PMC
Fadzil M.A.M., Mustar S., Rashed A.A. The Potential Use of Honey as a Neuroprotective Agent for the Management of Neurodegenerative Diseases. Nutrients. 2023;15:1558. doi: 10.3390/nu15071558. PubMed DOI PMC
Che Mohd Nassir C.M.N., Abdul Hamid H., Hambali A., Abd Manan N., Mehat M.Z., Ismail N.I., Mustapha M. Neuroprotective Potentials of Honey for Cerebral Small Vessel Disease. OBM Neurobiol. 2022;6:144. doi: 10.21926/obm.neurobiol.2204144. DOI
Nweze J.A.A., Nweze E.I., Olovo C.V., Obi O.J., Chidebelu P. Therapeutic Properties of Honey. IntechOpen; London, UK: 2019.
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. doi: 10.1038/s41598-018-27449-3. PubMed DOI PMC
Tsavea E., Vardaka F.-P., Savvidaki E., Kellil A., Kanelis D., Bucekova M., Grigorakis S., Godocikova J., Gotsiou P., Dimou M., et al. Physicochemical Characterization and Biological Properties of Pine Honey Produced across Greece. Foods. 2022;11:943. doi: 10.3390/foods11070943. PubMed DOI PMC
FAO. WHO Search Results. CODEXALIMENTARIUS. [(accessed on 8 May 2024)]. Available online: https://www.fao.org/fao-who-codexalimentarius/search/en/?cx=018170620143701104933%3Aqq82jsfba7w&q=honey&cof=FORID%3A9.
European Parliament . Council Directive 2001/110/EC of 20 December 2001 Relating to Honey. Volume 10 European Parliament; Strasbourg, France: 2001.
Vyhláška 76/2003 Sb., Kterou se Stanoví Požadavky pro Přírodní Sladidla, Med, Cukrovinky, Kakaový Prášek a Směsi. [(accessed on 24 April 2024)]. Available online: https://www.zakonyprolidi.cz/cs/2003-76.
Chakir A., Romane A., Marcazzan G.L., Ferrazzi P. Physicochemical Properties of Some Honeys Produced from Different Plants in Morocco. Arab. J. Chem. 2016;9:S946–S954. doi: 10.1016/j.arabjc.2011.10.013. DOI
Kirs E., Pall R., Martverk K., Laos K. Physicochemical and Melissopalynological Characterization of Estonian Summer Honeys. Procedia Food Sci. 2011;1:616–624. doi: 10.1016/j.profoo.2011.09.093. DOI
EU Pesticides Database-MRLs. [(accessed on 11 May 2024)]. Available online: https://ec.europa.eu/food/plant/pesticides/eu-pesticides-database/start/screen/mrls.
Gunes E., Şahin S., Demir C., Borum E., Bilisik Tosunoglu A. Determination of Phenolic Compounds Profile in Chestnut and Floral Honeys and Their Antioxidant and Antimicrobial Activities: Güneş et Al. J. Food Biochem. 2016;41:e12345. doi: 10.1111/jfbc.12345. DOI
Jibril F., Abu Bakar M.H., Manivannan L. Isolation and Characterization of Polyphenols in Natural Honey for the Treatment of Human Diseases. Bull. Natl. Res. Cent. 2019;43:4. doi: 10.1186/s42269-019-0044-7. DOI
Estevinho L., Pereira A.P., Moreira L., Dias L.G., Pereira E. Antioxidant and Antimicrobial Effects of Phenolic Compounds Extracts of Northeast Portugal Honey. Food Chem. Toxicol. 2008;46:3774–3779. doi: 10.1016/j.fct.2008.09.062. PubMed DOI
Lou Z., Wang H., Zhu S., Ma C., Wang Z. Antibacterial Activity and Mechanism of Action of Chlorogenic Acid. J. Food Sci. 2011;76:M398–M403. doi: 10.1111/j.1750-3841.2011.02213.x. PubMed DOI
Eumkeb G., Siriwong S., Phitaktim S., Rojtinnakorn N., Sakdarat S. Synergistic Activity and Mode of Action of Flavonoids Isolated from Smaller Galangal and Amoxicillin Combinations against Amoxicillin-Resistant Escherichia coli. J. Appl. Microbiol. 2012;112:55–64. doi: 10.1111/j.1365-2672.2011.05190.x. PubMed DOI
Grigoryan K. Chapter 12-Safety of Honey. In: Prakash V., Martín-Belloso O., Keener L., Astley S., Braun S., McMahon H., Lelieveld H., editors. Regulating Safety of Traditional and Ethnic Foods. Academic Press; San Diego, CA, USA: 2016. pp. 217–246.
Habib H.M., Al Meqbali F.T., Kamal H., Souka U.D., Ibrahim W.H. Physicochemical and Biochemical Properties of Honeys from Arid Regions. Food Chem. 2014;153:35–43. doi: 10.1016/j.foodchem.2013.12.048. PubMed DOI
Bucekova M., Bugarova V., Godocikova J., Majtan J. Demanding New Honey Qualitative Standard Based on Antibacterial Activity. Foods. 2020;9:1263. doi: 10.3390/foods9091263. PubMed DOI PMC
Ng W.-J., Sit N.-W., Ooi P.A.-C., Ee K.-Y., Lim T.-M. The Antibacterial Potential of Honeydew Honey Produced by Stingless Bee (Heterotrigona itama) against Antibiotic Resistant Bacteria. Antibiotics. 2020;9:871. doi: 10.3390/antibiotics9120871. PubMed DOI PMC
Baloš M., Popov N., Vidakovic Knezevic S., Ljubojević Pelić D., Pelić M., Mihaljev Ž., Jakšić S. Electrical Conductivity and Acidity of Honey. Arch. Vet. Med. 2018;11:91–101. doi: 10.46784/e-avm.v11i1.20. DOI
Masoura M., Passaretti P., Overton T.W., Lund P.A., Gkatzionis K. Use of a Model to Understand the Synergies Underlying the Antibacterial Mechanism of H2O2-Producing Honeys. Sci. Rep. 2020;10:17692. doi: 10.1038/s41598-020-74937-6. PubMed DOI PMC
Bugarova V., Godocikova J., Bucekova M., Brodschneider R., Majtan J. Effects of the Carbohydrate Sources Nectar, Sucrose and Invert Sugar on Antibacterial Activity of Honey and Bee-Processed Syrups. Antibiotics. 2021;10:985. doi: 10.3390/antibiotics10080985. PubMed DOI PMC
Kubo T., Sasaki M., Nakamura J., Sasagawa H., Ohashi K., Takeuchi H., Natori S. Change in the Expression of Hypopharyngeal-Gland Proteins of the Worker Honeybees (Apis mellifera L.) with Age and/or Role. J. Biochem. 1996;119:291–295. doi: 10.1093/oxfordjournals.jbchem.a021237. PubMed DOI
Bucekova M., Valachova I., Kohutova L., Prochazka E., Klaudiny J., Majtan J. Honeybee Glucose Oxidase--Its Expression in Honeybee Workers and Comparative Analyses of Its Content and H2O2-Mediated Antibacterial Activity in Natural Honeys. Naturwissenschaften. 2014;101:661–670. doi: 10.1007/s00114-014-1205-z. PubMed DOI
Weston R.J. The Contribution of Catalase and Other Natural Products to the Antibacterial Activity of Honey: A Review. Food Chem. 2000;71:235–239. doi: 10.1016/S0308-8146(00)00162-X. DOI
Dustmann: Über Die Katalaseaktivität in Bienenhonig-Google Scholar. [(accessed on 11 May 2024)]. Available online: https://scholar.google.com/scholar_lookup?title=%C3%9Cber%20die%20Katalaseaktivit%C3%A4t%20in%20Bienenhonig%20aus%20der%20Tracht%20der%20Heidekrautgew%C3%A4chse%20&publication_year=1971&author=J.H.%20Dustman.
Tomás-Barberán F., Martos I., Ferreres F., Radovic B., Anklam E. HPLC Flavonoid Profile as Markers for the Botanical Origin of European Honey. J. Sci. Food Agric. 2001;81:485–496. doi: 10.1002/jsfa.836. DOI
Nešović M., Gašić U., Tosti T., Trifković J., Baošić R., Blagojević S., Ignjatović L., Tešić Ž. Physicochemical Analysis and Phenolic Profile of Polyfloral and Honeydew Honey from Montenegro. RSC Adv. 2020;10:2462–2471. doi: 10.1039/C9RA08783D. PubMed DOI PMC
Kurek-Górecka A., Górecki M., Rzepecka-Stojko A., Balwierz R., Stojko J. Bee Products in Dermatology and Skin Care. Molecules. 2020;25:556. doi: 10.3390/molecules25030556. PubMed DOI PMC
Bellion P., Olk M., Will F., Dietrich H., Baum M., Eisenbrand G., Janzowski C. Formation of Hydrogen Peroxide in Cell Culture Media by Apple Polyphenols and Its Effect on Antioxidant Biomarkers in the Colon Cell Line HT-29. Mol. Nutr. Food Res. 2009;53:1226–1236. doi: 10.1002/mnfr.200800456. PubMed DOI
Kędzierska-Matysek M., Florek M., Wolanciuk A., Barłowska J., Litwińczuk Z. Concentration of Minerals in Nectar Honeys from Direct Sale and Retail in Poland. Biol. Trace Elem. Res. 2018;186:579–588. doi: 10.1007/s12011-018-1315-0. PubMed DOI PMC
Rt A., Bogdanov S., Haldimann M., Luginbühl W., Gallmann P. Minerals in Honey: Environmental, Geographical and Botanical Aspects. J. Apic. Res. Bee World. 2007;46:269–275. doi: 10.3896/IBRA.1.46.4.11. DOI
Kurek-Górecka A., Rzepecka-Stojko A., Górecki M., Stojko J., Sosada M., Świerczek-Zięba G. Structure and Antioxidant Activity of Polyphenols Derived from Propolis. Molecules. 2014;19:78–101. doi: 10.3390/molecules19010078. PubMed DOI PMC
Rane M., Deshmukh K., Mulik P., Mulani N., Patwardhan R. Resolving a Mechanism of Honey Antibacterial Action: Polyphenol/H2O2-Induced Oxidative Effect on Bacterial Cell Growth and on DNA Degradation. Indian J. Appl. Pure Bio. 2021;36:1–10.
Brudzynski K., Abubaker K., Laurent M., Castle A. Re-Examining the Role of Hydrogen Peroxide in Bacteriostatic and Bactericidal Activities of Honey. Front. Microbiol. 2011;2:213. doi: 10.3389/fmicb.2011.00213. PubMed DOI PMC
Bucekova M., Juricova V., Di Marco G., Gismondi A., Leonardi D., Canini A., Majtan J. Effect of Thermal Liquefying of Crystallised Honeys on Their Antibacterial Activities. Food Chem. 2018;269:335–341. doi: 10.1016/j.foodchem.2018.07.012. PubMed DOI
González-Miret M.L., Terrab A., Hernanz D., Fernández-Recamales M.A., Heredia F.J. Multivariate Correlation between Color and Mineral Composition of Honeys and by Their Botanical Origin. J. Agric. Food Chem. 2005;53:2574–2580. doi: 10.1021/jf048207p. PubMed DOI
Škrovánková S., Snopek L., Mlček J., Volaří ková E. Bioactive Compounds Evaluation in Different Types of Czech and Slovak Honeys. Potr. S. J. F. Sci. 2019;13:94–99. doi: 10.5219/1025. DOI