Property-Wound Healing Relationship of Manuka-, Anzer- and Chestnut-Honey: Characterization, Antibacterial Properties and Cell Culture Applications
DOI:
https://doi.org/10.24925/turjaf.v12i10.1826-1834.6869Keywords:
Chestnut honey, Honey, Anti-oxidant activity, Wound healing , Antioxidant activityAbstract
Honey is known to be a natural food product with antibacterial and wound-healing properties. Among its different types, some attributed more with medical applications including Manuka honey. In this study, some wound healing-related parameters were systematically investigated on two different types of Turkish honey (Chestnut and Anzer), in comparison with Manuka honey. Chestnut honey had considerable amount of hydrogen peroxide (5 μg/mL) whereas Manuka and Anzer honey did not contain any. Additionally, Chestnut honey had the highest acidity among all tested samples (24.50 meq/kg), as well as higher antioxidant activity (IC50 ; 2.45 mg/ml) than those of Anzer (13.02 mg/ml) and Manuka honey (6.27 mg/ml). It was also demonstrated that Chestnut honey displayed a considerable antimicrobial activity against selected pathogens. On the other hand, in the scratch assay performed as a model for the wound healing process, Anzer honey induced the highest cell proliferation corresponding to almost total wound closure for all concentrations tested. Overall, the results showed that the Turkish Chestnut and Anzer honey samples had distinguished characteristics for wound healing that is comparable to Manuka honey, and therefore are both promising candidates for use in clinical applications.
References
Abd El-Aziz, MA, Elbadry, S, Samy, HM, Tamer, TM, 2022. Prevalence, antimicrobial resistance profile, and characterization of multi-drug resistant bacteria from various infected wounds in North Egypt. Saudi Journal of Biological Sciences, 29: 2978–2988.
Aker, D, Nisbet, C, 2020. Antioxidant activities, total phenolic and flavonoid contents of honey collected from different botanical origins. Ankara Universitesi Veteriner Fakultesi Dergisi, 67: 133–136. doi:10.33988/auvfd.523745
Al-Waili, NS, Salom, K, Al-Ghamdi, AA, 2011. Honey for wound healing, ulcers, and burns; data supporting its use in clinical practice. TheScientificWorldJournal, 11: 766–787. doi:10.1100/tsw.2011.78
Albaridi, NA, 2019a. Antibacterial potency of honey. International journal of microbiology, 1: 2464507.
Albaridi, NA, 2019b. Antibacterial Potency of Honey. International Journal of Microbiology, 2019:. doi:10.1155/2019/2464507
Almasaudi, S, 2021. The antibacterial activities of honey. Saudi Journal of Biological Sciences, 28: 2188–2196. doi:10.1016/j.sjbs.2020.10.017
AOAC, 1990. Official methods of analysis of the AOAC. In: Methods. Association of official analytical chemists, Arlington, VA, USA, pp. 932.06, 925.09, 985.29, 923.03.
Ball, DW, 2006. Concentration Scales for Sugar Solutions. Journal of Chemical Education, 83:.
Basualdo, C, Sgroy, V, Finola, MS, Marioli, JM, 2007. Comparison of the antibacterial activity of honey from different provenance against bacteria usually isolated from skin wounds. Veterinary Microbiology, 124: 375–381. doi:10.1016/j.vetmic.2007.04.039
Bazaid, AS, Aldarhami, A, Patel, M, Adnan, M, Hamdi, A, Snoussi, M, Khateb, AM, 2022. The antimicrobial effects of Saudi sumra honey against drug resistant pathogens: phytochemical analysis, antibiofilm, anti-quorum sensing, and antioxidant activities. Pharmaceuticals, 15: 1212.
Bernstein, RC, 2013. The Science Journal of the Lander College of Arts and Sciences The Scientific Evidence Validating The Use of Honey as a Medicinal Agent 6:.
Blair, SE, Carter, DA, 2005. The potential for honey in the management of wounds and infection. Australian Infection Control, 10: 24–31. doi:10.1071/hi05024
Brudzynski, K, 2021. Honey as an ecological reservoir of antibacterial compounds produced by antagonistic microbial interactions in plant nectars, honey and honey bee. Antibiotics, 10: 551.
Carlo, G Di, Mascolo, N, Izzo, AA, Capasso, F, 1999. Flavonoids: old and new aspects of a class of natural therapeutic drugs. Life Sciences, 65: 337–353.
Carvalho, MTB, Araújo-Filho, HG, Barreto, AS, Quintans-Júnior, LJ, Quintans, JSS, Barreto, RSS, 2021. Wound healing properties of flavonoids: A systematic review highlighting the mechanisms of action. Phytomedicine, 90:. doi:10.1016/j.phymed.2021.153636
Chijioke, OC, Aliyu, RM, Ohams, OE, Onyebuchi, AD, Fountain, AI, Nwaforcha, NB, 2023. Natural honey and diabetic wound healing: A review of literature. Magna Scientia Advanced Research and Reviews, 7: 067–073.
Combarros-Fuertes, P, Fresno, JM, Estevinho, MM, Sousa-Pimenta, M., Tornadijo, M. E., Estevinho, LM, 2020. Honey: another alternative in the fight against antibiotic-resistant bacteria? Antibiotics, 9: 774.
Dağ, B, Sıralı, R, Tarakçı, Z, 2017. Investigation Of Some Properties Of Chestnut Honey Produced In Black Sea Region Of Turkey. Batman University Journal of Life Sciences, 7: 118–123.
Denny, KJ, Wale, J De, B., LK, Harris, PN, Lipman, J, 2020. When not to start antibiotics: avoiding antibiotic overuse in the intensive care unit. Clinical Microbiology and Infection, 26: 35–40.
Derebaşı, E, Bulut, G, Col, M, Güney, F, Yaşar, N, Ertürk, Ö, 2014. Physicochemical and residue analysis of honey from Black Sea Region of Turkey. Fresenius Environmental Bulletin, 23: 10–17.
El-Senduny, FF, Hegazi, NM, Abd Elghani, GE, Farag, MA, 2021. Manuka honey, a unique mono-floral honey. A comprehensive review of its bioactives, metabolism, action mechanisms, and therapeutic merits. Food Bioscience, 42: 101038. doi:10.1016/j.fbio.2021.101038
Ergene, E, Sezlev Bilecen, D, Kaya, B, Yilgor Huri, P, Hasirci, V, 2020. 3D cellular alignment and biomimetic mechanical stimulation enhance human adipose-derived stem cell myogenesis. Biomedical Materials (Bristol), 15:. doi:10.1088/1748-605X/ab95e2
Eroglu, O, Deniz, T, Kisa, U, Comu, FM, Kaygusuz, S, Kocak, OM, 2018. The effect of different types of honey on healing infected wounds. Journal of Wound Care, 27: 18–25.
EU Council, 2002. Council directive 2001/11 O/EC of 20 December 2001 relating to honey. Official Journal of European Communities, 10: 42–57.
Feng, Y, Sanders, AJ, Morgan, LD, Harding, KG, Jiang, WG, 2016. Potential roles of suppressor of cytokine signaling in wound healing. Regen Med, 11: 193–209.
Foschi, D, Yakushkina, A. O., Cammarata, F, Lamperti, G, Colombo, F, Rimoldi, S, Sampietro, GM, 2022. Surgical site infections caused by multi-drug resistant organisms: A case–control study in general surgery. Updates in Surgery, 74: 1763–1771.
Frydman, GH, Olaleye, D, Annamalai, D, Layne, K, Yang, I, Kaafarani, HM, Fox, JG, 2020. Manuka honey microneedles for enhanced wound healing and the prevention and/or treatment of Methicillin-resistant Staphylococcus aureus (MRSA) surgical site infection. Scientific reports, 10: 13229.
Gençay Çelemli̇, Ö, Pınar BARKAN, N, Özeni̇rler, Ç, Özel Demi̇ralp, D, Sorkun, K, 2017. Protein Analysis of Anzer Bee Pollen by Bradford Method. Mellifera, 17: 21–32.
Girma, A, Seo, W, SheI, RC, 2019. Antibacterial activity of varying UMF-graded Manuka honeys. PLoS ONE, 14: 1–9. doi:10.1371/journal.pone.0224495
Gobin, I, Crnković, G, Magdalenić, M, Begić, G, Babić, A, Lušić, D, Vučković, D, 2018. Antibacterial potential of Croatian honey against antibiotic resistant pathogenic bacteria. Antibiotics, 15: 139–144.
Güneş, ME, Şahin, S, Demir, C, Borum, E, Tosunoğlu, A, 2017. Determination of phenolic compounds profile in chestnut and floral honeys and their antioxidant and antimicrobial activities. Journal of Food Biochemistry, 41: 1–12. doi:10.1111/jfbc.12345
Helrich, K, 1990. Official methods of analysis of the association of official analytical chemists, 15th ed. Association of Official Analytical Chemists Inc., Arlington.
Hepsağ, F, 2019. Determination of total phenolic compounds and antioxidant capacity of Anzer honey produced in Rize, Turkey. The Journal of Food, 44: 641–653. doi:10.15237/gida.gd19046
Hossain, ML, Lim, LY, Hammer, K, Hettiarachchi, D, Locher, C, 2022. A review of commonly used methodologies for assessing the antibacterial activity of honey and honey products. Antibiotics, 11: 975.
Johnston, M, McBride, M, Dahiya, D, Owusu-Apenten, R, Singh Nigam, P, 2018. Antibacterial activity of Manuka honey and its components: An overview. AIMS Microbiology, 4: 655–664. doi:10.3934/microbiol.2018.4.655
Kapoor, N, Yadav, R, 2021. Manuka honey: A promising wound dressing material for the chronic nonhealing discharging wounds: A retrospective study. National journal of maxillofacial surgery, 12: 233–237.
Kara, Y, 2020. Phenolic Composition of Pine (Pinus spp.) Honey from Turkey. Journal of Apitherapy and Nature, 2: 52–58.
Kirkpatrick, G, Nigam, P, Owusu-Apenten, R, 2017. Total Phenols, Antioxidant Capacity and Antibacterial Activity of Manuka Honey Chemical Constituents. Journal of Advances in Biology & Biotechnology, 15: 1–7. doi:10.9734/jabb/2017/37242
Kolaylı, S, Kongur, N, Gundogdu, A, Kemer, B, Duran, C, Yazicioglu, R, 2008. Mineral composition of selected honeys from Turkey. Asian Journal of Chemistry, 20: 2421–2425.
Komolafe, O, 2004. Antibiotic resistance in bacteria - an emerging public health problem. Malawi Medical Journal,. doi:10.4314/mmj.v15i2.10780
Krishnakumar, GS, Mahendiran, B, Gopalakrishnan, S, Muthusamy, S, Malarkodi Elangovan, S, 2020. Honey based treatment strategies for infected wounds and burns: A systematic review of recent pre-clinical research. Wound Medicine, 30: 100188. doi:10.1016/j.wndm.2020.100188
Kuropatnicki, AK, Kłósek, M, Kucharzewski, M, 2018. La miel como medicina. Perspectivas históricas. Journal of Apicultural Research, 57: 113–118. doi:10.1080/00218839.2017.1411182
Kwakman, PHS, Velde, AA te, Boer, L de, Vandenbroucke-Grauls, CMJE, Zaat, SAJ, 2011. Two major medicinal honeys have different mechanisms of bactericidal activity. PLoS ONE, 6: 3–9. doi:10.1371/journal.pone.0017709
Malkoç, M, Çakir, H, Kara, Y, Can, Z, Kolayli, S, 2019. Phenolic composition and antioxidant properties of Anzer honey from Black Sea region of Turkey. Uludağ Bee Journal, 19: 143–151.
Martin, PG, 1979. Manuals of Food Quality Control: 3. Commodities. Food and Agriculture Organization of the United Nations, Rome.
Maruhashi, E, 2020. Honey in Wound Healing The History of Honey. In: Boateng, J. (Ed.), Therapeutic Dressings and Wound Healing Applications. John Wiley and Sons, pp. 235–254.
Matzen, RD, Leth-Espensen, JZ, Jansson, T, Nielsen, DS, Lund, MN, Matzen, S, 2018. The Antibacterial Effect in Vitro of Honey Derived from Various Danish Flora. Dermatology Research and Practice, 2018:. doi:10.1155/2018/7021713
Menezes, P do. P, Frank, LA, Lima, B do. S, Carvalho, YMBG de, Serafini, MR, Quintas-Junior, LJ, Pohlmnn, A. R., Guterres, S. S., Araujo, AA de S, 2017. Hesperetin-loaded lipid-core nanocapsules in polyamide: a new textile formulation for topical drug delivery. Int. J. Nanomed, 12: 2069–2079.
Mihai, MM, Dima, MB, Dima, B, Holban, AM, 2019. Nanomaterials for Wound Healing and Infection Control. Materials, 12: 2176. doi:Mara Madalina Mihai
Minden-Birkenmaier, BA, Bowlin, GL, 2018. Honey-based templates in wound healing and tissue engineering. Bioengineering, 5:. doi:10.3390/bioengineering5020046
Mssillou, I, Bakour, M, Slighoua, M, Laaroussi, H., Saghrouchni, H, Amrati, FEZ, Derwich, E, 2022. Investigation on wound healing effect of Mediterranean medicinal plants and some related phenolic compounds: A review. Journal of ethnopharmacology, 298
Napavichayanun, S, Aramwit, P, 2017. Effect of animal products and extracts on wound healing promotion in topical applications: a review. Journal of Biomaterials Science, Polymer Edition, 28: 703–729. doi:10.1080/09205063.2017.1301772
Nolan, VC, Harrison, J, Wright, JEE, Cox, JAG, 2020. Clinical significance of manuka and medical-grade honey for antibiotic-resistant infections: A systematic review. Antibiotics, 9: 1–24. doi:10.3390/antibiotics9110766
Onbas, T, Osmanagaoglu, O, Kiran, F, 2018. Potential Properties of Lactobacillus plantarum F-10 as a Bio-control Strategy for Wound Infections. Probiotics and Antimicrobial Proteins, 11: 1110–1123.
Oryan, A, Alemzadeh, E, Moshiri, A, 2016. Biological properties and therapeutic activities of honey in wound healing: A narrative review and meta-analysis. Journal of Tissue Viability, 25: 98–118. doi:10.1016/j.jtv.2015.12.002
Özkök, A, D’arcy, B, Sorkun, K, 2010. Total Phenolic Acid and Total Flavonoid Content of Turkish Pine Honeydew Honey. Journal of Apiproduct and Apimedical Science, 2: 65–71.
Pasupuleti, VR, Arigela, CS, Gan, SH, Salam, SKN, Krishnan, KT, Rahman, NA, Jeffree, MS, 2020. A review on oxidative stress, diabetic complications, and the roles of honey polyphenols. Oxidative medicine and cellular longevity, 1: 8878172.
Puca, V, Marulli, RZ, Grande, R, Vitale, I, Niro, A, Molinaro, G, Giovanni, P Di, 2021. Microbial species isolated from infected wounds and antimicrobial resistance analysis: Data emerging from a three-years retrospective study. Antibiotics, 10: 1162.
Pushpavalli, G, Kalaiarasi, P, Veeramani, C, Pugalendi, KV, 2010. Effect of chrysin on hepatoprotective and antioxidant status in D-galactosamine-induced hepatitis in rats. Eur. J. Pharmacol., 631: 36–41.
Rodriguez, L, Wu, X, Guan, JL, 2005. Wound-healing assay. Methods in Molecular Biology, 294: 23–29.
Saikaly, SK, Khachemoune, A, 2017. Honey and Wound Healing: An Update. American Journal of Clinical Dermatology, 18: 237–251. doi:10.1007/s40257-016-0247-8
Samatha, T, Shyamsundarachary, R, Srinivas, P, Swang, N., R, 2012. Quantification of total phenolic and total flavonoid contents in extracts of Oroxylum indicum L. Kurz. Asian Journal of Pharmaceutical and. Clinical Research, 5:.
Scepankova, H, Combarros-Fuertes, P, Fresno, JM, Tornadijo, ME, Dias, MS, Pinto, CA, Estevinho, LM, 2021. Role of honey in advanced wound care. Molecules, 26: 4784.
Shallcross, LJ, Davies, DSC, 2014. Antibiotic overuse: a key driver of antimicrobial resistance. British Journal of General Practice, 64: 604–605.
Strelec, I, Crevar, B, Kovac, T, Bilic Rajs, B, Primorac, L, Flanjak, I, 2018. Glucose oxidase activity and hydrogen peroxide accumulation in Croatian honeys. Croatian Journal of Food Science and Technology, 10: 33–41. doi:10.17508/cjfst.2018.10.1.06
Subramanian, S, Duraipandian, C, Alsayari, A, Ramachawolran, G, Wong, LS, Sekar, M, Wahab, S, 2023. Wound healing properties of a new formulated flavonoid-rich fraction from Dodonaea viscosa Jacq. leaves extract. Frontiers in Pharmacology, 14: 1096905.
Tashkandi, H, 2021. Honey in wound healing: An updated review. Open life sciences, 16: 1091–1100.
Tezcan, F, Kolayli, S, Ulusoy, HSE, Erim, FB, 2011. Evaluation of organic acid, saccharide composition and antioxidant properties of some authentic Turkish honeys. Journal of Food and Nutrition Research, 50: 33–40.
Wadi, MA, 2022. In Vitro Antibacterial Activity of Different Honey Samples against Clinical Isolates. BioMed Research International, 2022:. doi:10.1155/2022/1560050
Willix, DJ, Molan, PC, Harfoot, CG, 1992. A comparison of the sensitivity of wound-infecting species of bacteria to the antibacterial activity of manuka honey and other honey. Journal of Applied Microbiology, 73: 388–394.
Yang, X, Fan, L, Ma, L, Wang, Y, Lin, S, Yu, F, Pan, X, Luo, G, Zhang, D, Wang, H, 2017. Green electrospun Manuka honey/silk fibroin fibrous matrices as potential wound dressing. Materials and Design, 119: 76–84. doi:10.1016/j.matdes.2017.01.023
Yilmaz, AC, Aygin, D, 2020. Honey dressing in wound treatment: a systematic review. Complementary therapies in medicine, 51: 102388.
Yupanqui Mieles, J, Vyas, C, Aslan, E, Humphreys, G, Diver, C, Bartolo, P, 2022. Honey: An advanced antimicrobial and wound healing biomaterial for tissue engineering applications. Pharmaceuticals, 14: 1663.
Downloads
Published
How to Cite
Issue
Section
License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
