The quality of Slovenian chestnut honey and its specific properties relevant for medical application and functional nutrition

Authors

  • Janko Božič
  • Jasna Bertoncelj
  • Damjana Drobne
  • Gordana Glavan
  • Nina Gunde Cimerman
  • Adrijana Leonardi
  • Rok Kopinč
  • Anita Jemec Kokalj
  • Sara Novak
  • Mojca Korošec
  • Igor Križaj
  • Blaž Podrižnik
  • Martina Turk
  • Andrej Zabret

DOI:

https://doi.org/10.14720/abs.63.2.15935

Keywords:

antimicrobial activity, antioxidant activity, kynurenic acid, honey contamination, melissopalinology, organic honey

Abstract

Chestnut honey is well-described in terms of sensory properties, pollen and chemical composition. Specific bitter taste is accompanied with other typical sensory properties derived from its chemical composition, especially in the nectar of sweet chestnut. Compounds from other sources of nectar and honeydew, especially linden, fir and spruce, with smaller amounts from meadow plants, create the specific sensory and chemical properties of Slovene chestnut honey. Based on the chemical composition of the honey, especially the content and proportions of different inorganic ions, it is possible to track the geographical origin of the pasture. Bees contribute significantly to recognized antimicrobial properties of honey by secretion of enzymes and antimicrobial peptides via the food processing glands. When the honey is used for medical purposes, we have to take precautions to avoid microbial and chemical contamination. For the planning of specific use of honey as a medical application we need to explore in detail specific pharmacological properties of single compounds from the chestnut honey and its contribution to the whole activity during wound treatment. In this paper we present a review of most distinct properties of chestnut honey important for its medical application.

References

Al-Waili, N., Salom, K., Al-Ghamdi, A., Ansari, M.J., 2012. Antibiotic, Pesticide, and Microbial Contaminants of Honey: Human Health Hazards. The Scientific World Journal 2012, 1–9. DOI: https://doi.org/10.1100/2012/930849

Beretta, G., Artali, R., Caneva, E., Orlandini, S., Centini, M., Facino, R.M., 2009. Quinoline alkaloids in honey: Further analytical (HPLC-DAD-ESI-MS, multidimensional diffusion-ordered NMR spectroscopy), theoretical and chemometric studies. Journal of Pharmaceutical and Biomedical Analysis, 50, 432–439. DOI: https://doi.org/10.1016/j.jpba.2009.05.029

Bertoncelj, J., Golob, T., Kropf, U., Korošec, M., 2011a. Characterisation of Slovenian honeys on the basis of sensory and physicochemical analysis with a chemometric approach. International Journal of Food Science & Technology, 46, 1661–1671. DOI: https://doi.org/10.1111/j.1365-2621.2011.02664.x

Bertoncelj, J., Polak, T., Kropf, U., Korošec, M., Golob, T., 2011b. LC-DAD-ESI/MS analysis of flavonoids and abscisic acid with chemometric approach for the classification of Slovenian honey. Food Chemistry, 127, 296–302. DOI: https://doi.org/10.1016/j.foodchem.2011.01.003

Bilikova, K., Krakova, T.K., Yamaguchi, K., Yamaguchi, Y., 2015. Major royal jelly proteins as markers of authenticity and quality of honey. Archives of Industrial Hygiene and Toxicology, 66, 259–267. DOI: https://doi.org/10.1515/aiht-2015-66-2653

Bogdanov, S., Ruoff, K., Oddo, L.P., 2004. Physico-chemical methods for the characterisation of unifloral honeys: a review. Apidologie, 35, S4–S17. DOI: https://doi.org/10.1051/apido:2004047

Bucekova, M., Buriova, M., Pekarik, L., Majtan, V., Majtan, J., 2018. Phytochemicals-mediated production of hydrogen peroxide is crucial for high antibacterial activity of honeydew honey. Scientific Reports, 8, 9061. DOI: https://doi.org/10.1038/s41598-018-27449-3

Bucekova, M., Sojka, M., Valachova, I., Martinotti, S., Ranzato, E., Szep, Z., Majtan, V., Klaudiny, J., Majtan, J., 2017. Bee-derived antibacterial peptide, defensin-1, promotes wound re-epithelialisation in vitro and in vivo. Scientific Reports, 7, 7340. DOI: https://doi.org/10.1038/s41598-017-07494-0

Bucekova, M., Valachova, I., Kohutova, L., Prochazka, E., Klaudiny, J., Majtan, J., 2014. Honeybee glucose oxidase—its expression in honeybee workers and comparative analyses of its content and H2O2-mediated antibacterial activity in natural honeys. Naturwissenschaften, 101, 661–670. DOI: https://doi.org/10.1007/s00114-014-1205-z

Buttstedt, A., Moritz, R.F.A., Erler, S., 2014. Origin and function of the major royal jelly proteins of the honeybee (Apis mellifera) as members of the yellow gene family. Biological Reviews, 89, 255–269. DOI: https://doi.org/10.1111/brv.12052

Casteels, P., Ampe, C., Jacobs, F., Tempst P., 1993. Functional and chemical characterization of Hyme- noptaecin, an antibacterial polypeptide that is infection-inducible in the honeybee (Apis mellifera). DOI: https://doi.org/10.1016/S0021-9258(18)53143-4

The Journal of Biological Chemistry, 268, 7044–7054.

Casteels, P., Ampe, C., Rivière, L., Van Damme, J., Elicone, C., Fleming, M., Jacobs, F., Tempst P., 1990. Isolation and characterization of abaecin, a major antibacterial response peptide in the honeybee (Apis mellifera). European Journal of Biochemistry, 187, 381–386. DOI: https://doi.org/10.1111/j.1432-1033.1990.tb15315.x

Česnik, H.B., Kmecl, V., Bolta, Š.V., 2019. Pesticide and veterinary drug residues in honey - validation of methods and a survey of organic and conventional honeys from Slovenia. Food Additives & Contaminants: Part A, 36, 1358–1375. DOI: https://doi.org/10.1080/19440049.2019.1631492

Council Directive, 1974. 74/409/EEC of 22 July. On harmonization of the laws of the member states relating to honey. Offcial Journal of the European Communities 17, 10–14.

Crailsheim, K., 1991. Interadult feeding of jelly in honeybee (Apis mellifera L.) colonies. Journal of Comparative Physiology B, 161, 55–60. DOI: https://doi.org/10.1007/BF00258746

Erban, T., Shcherbachenko, E., Talacko, P., Harant, K., 2019. The unique protein composition of honey revealed by comprehensive proteomic analysis: Allergens, venom-like proteins, antibacterial properties, royal jelly proteins, serine proteases, and their inhibitors. Journal of Natural Products, 82, 1217–1226. DOI: https://doi.org/10.1021/acs.jnatprod.8b00968

European Commission, 2018. Technical guidelines for determining the magnitude of pesticide residues in honey and setting maximum residue levels in honey. SANTE/11956/2016 rev.9, pp. 41.

Feng, M., Fang, Y., Han, B., Zhang, L., Lu, X., Li, J., 2013. Novel aspects of understanding molecular working mechanisms of salivary glands of worker honeybees (Apis mellifera) investigated by proteomics and phosphoproteomics. Journal of Proteomics, 87, 1–15. DOI: https://doi.org/10.1016/j.jprot.2013.05.021

Fontana, R., Mendes, M.A., Souza, B.M., Konno, K., César, L.M.M., Malaspina, O., Palma M.S., 2004. Jelleines: a family of antimicrobial peptides from the royal jelly of honeybees (Apis mellifera). Peptides, 25, 919–928. DOI: https://doi.org/10.1016/j.peptides.2004.03.016

Fujita, T., Kozuka-Hata, H., Uno, Y., Nishikori, K., Morioka, M., Oyama, M., Kubo, T., 2010. Functional analysis of the honeybee (Apis mellifera L.) salivary system using proteomics. Biochemical and Biophysical Research Communications, 397, 740–744. DOI: https://doi.org/10.1016/j.bbrc.2010.06.023

Fujiwara, S., Imai, J., Fujiwara, M., Yaeshima, T., Kawashima, T., Kobayashi, K., 1990. A potent anti- bacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. Journal of Biological Chemistry, 265, 11333–11337. DOI: https://doi.org/10.1016/S0021-9258(19)38596-5

Golob, T., Korošec, M., Bertoncelj, J., Kropf, U., Kandolf Borovšak, A., Božič, J., Zdešar, P., Meglič, M., Goljat, A., Šivic, F., Borovšak U., Veljanovski-Geremia, V., Sonc, C., Kandolf Borovšak, A., 2008. Med: značilnosti slovenskega medu. Čebelarska zveza Slovenije, Javna svetovalna služba v čebelarstvu, Lukovica.

Grabowski, N.T., Klein, G., 2017. Microbiology and foodborne pathogens in honey. Critical Reviews in Food Science and Nutrition, 57, 1852–1862.

Hermanns, R., Mateescu, C., Thrasyvoulou, A., Tananaki, C., Wagener, F.A.D.T.G., Cremers, N.A.J., 2020. Defining the standards for medical grade honey. Journal of Apicultural Research, 59, 125–135. DOI: https://doi.org/10.1080/00218839.2019.1693713

Huo, X., Wu, B., Feng, M., Han, B., Fang, Y., Hao, Y., Meng, L., Wubie, A.J., Fan, P., Hu, H., Qi, Y., Li, J., 2016. Proteomic analysis reveals the molecular underpinnings of mandibular gland development and lipid metabolism in two lines of honeybees (Apis mellifera ligustica). Journal of Proteome Research, 15, 3342–3357. DOI: https://doi.org/10.1021/acs.jproteome.6b00526

Ilyasov, R., Gaifullina, L., Saltykova, E., Poskryakov, A., Nikolenko, A., 2012. Review of the expression of antimicrobial peptide defensin in honey bees Apis mellifera L. Journal of Apicultural Science, 56, 115–124. DOI: https://doi.org/10.2478/v10289-012-0013-y

Janghu, S., Bera, M.B., Nanda, V., Rawson, A., 2017. Study on power ultrasound optimization and its comparison with conventional thermal processing for treatment of raw honey. Food Technology and Biotechnology, 55, 570–579. DOI: https://doi.org/10.17113/ftb.55.04.17.5263

Jo, C., Kim, J.K., Kang, H.J., Young, L.E., Byun, M.W., 2005. Irradiation effects on the decontamina- tion of microorganisms in honey. International Symposium »New frontiers of irradiated food and non-food products«, September 22-23, 2005, Gangkok, Thailand. pp. 8.

Kandolf, A., 2011. Pelodna analiza medu iz različnih fitogeografskih območij Slovenije = Pollen spectrum of honey from different phytogeographical areas of Slovenia. M. Sc. Thesis, University of Ljubljana, Biotechnical faculty.

Klaudiny, J., Albert, Š., Bachanová, K., Kopernický, J., Šimúth, J., 2005. Two structurally different defensin genes, one of them encoding a novel defensin isoform, are expressed in honeybee Apis mellifera. Insect Biochemistry and Molecular Biology, 35, 11–22. DOI: https://doi.org/10.1016/j.ibmb.2004.09.007

Korošec, M., Kandolf Borovšak, A., Božič, J., Bertoncelj, J., Justinek, J., Lilek, N., Kozmus, P., 2016a. Končno poročilo projekta Karakterizacija slovenskega medu / Final report of the project ‘Characte- risation of Slovene honey’. Čebelarska zveza Slovenije, Biotehniška fakulteta, Lukovica, Ljubljana. Korošec, M., Kropf, U., Golob, T., Bertoncelj, J., 2016b. Functional and nutritional properties of different types of slovenian honey. In: Kristbergsson, K., Ötles, S. (eds.): Functional Properties of Traditional Foods. Springer US, Boston, MA, pp. 323–338. DOI: https://doi.org/10.1007/978-1-4899-7662-8_23

Kropf, U., Korošec, M., Bertoncelj, J., Ogrinc, N., Nečemer, M., Kump, P., Golob, T., 2010. Deter- mination of the geographical origin of Slovenian black locust, lime and chestnut honey. Food Chemistry, 121, 839–846. DOI: https://doi.org/10.1016/j.foodchem.2009.12.094

Kubo, T., Sasaki, M., Nakamura, J., Sasagawa, H., Ohashi, K., Takeuchi, H., Natori, S., 1996. Change in the expression of hypopharyngeal-gland proteins of the worker honeybees (Apis mellifera L.) with age and/or role. The Journal of Biochemistry, 119, 291–295. DOI: https://doi.org/10.1093/oxfordjournals.jbchem.a021237

Kunčič, M.K., Jaklič, D., Lapanje, A., Gunde-Cimerman, N., 2012. Antibacterial and antimycotic activities of Slovenian honeys. British Journal of Biomedical Science, 69, 154–158. DOI: https://doi.org/10.1080/09674845.2012.12069144

Kwakman, P.H.S., Velde, A.A. te, Boer, L., de, Speijer, D., Vandenbroucke-Grauls, C.M.J.E., Zaat, S.A.J., 2010. How honey kills bacteria. The FASEB Journal, 24, 2576–2582. DOI: https://doi.org/10.1096/fj.09-150789

Kwakman, P.H.S., Velde, A.A. te, Boer, L., de, Vandenbroucke-Grauls, C.M.J.E., Zaat, S.A.J., 2011. Two major medicinal honeys have different mechanisms of bactericidal activity. PLoS ONE 6, e17709. DOI: https://doi.org/10.1371/journal.pone.0017709

Kwakman, P.H.S., Zaat, S.A.J., 2012. Antibacterial components of honey. IUBMB Life, 64, 48–55. Leyva-Daniel, D.E., Escobedo-Avellaneda, Z., Villalobos-Castillejos, F., Alamilla-Beltrán, L., Welti-Chanes, J., 2017. Effect of high hydrostatic pressure applied to a Mexican honey to increase its microbiological and functional quality. Food and Bioproducts Processing, 102, 299–306. DOI: https://doi.org/10.1016/j.fbp.2017.01.001

Małaczewska, J., Siwicki, A.K., Wójcik, R.M., Kaczorek, E., Turski, W.A., 2014. Effect of oral ad- ministration of kynurenic acid on the activity of the peripheral blood leukocytes in mice. Central- European Journal of Immunology, 39, 6–13. DOI: https://doi.org/10.5114/ceji.2014.42115

Martin, S.J., Correia-Oliveira, M.E., Shemilt, S., Drijfhout, F.P., 2018. Is the salivary gland associated with honey bee recognition compounds in worker honey bees (Apis mellifera)? Journal of Chemical Ecology, 44, 650–657. DOI: https://doi.org/10.1007/s10886-018-0975-8

Matysik-Woźniak, A., Paduch, R., Turski, W.A., Maciejewski, R., Jünemann, A.G., Rejdak, R., 2017. Effects of tryptophan, kynurenine and kynurenic acid exerted on human reconstructed corneal epithelium in vitro. Pharmacological Reports, 69, 722–729. DOI: https://doi.org/10.1016/j.pharep.2017.02.020

Mavric, E., Wittmann, S., Barth, G., Henle, T., 2008. Identification and quantification of methylglyoxal as the dominant antibacterial constituent of Manuka (Leptospermum scoparium) honeys from New Zealand. Molecular Nutrition & Food Research, 52, 483–489. DOI: https://doi.org/10.1002/mnfr.200700282

Milart, P., Paluszkiewicz, P., Dobrowolski, P., Tomaszewska, E., Smolinska, K., Debinska, I., Gawel, K., Walczak, K., Bednarski, J., Turska, M., Raba,n M., Kocki, T., Turski, W.A., 2019. Kynurenic acid as the neglected ingredient of commercial baby formulas. Scientific Reports, 9, 1–8. DOI: https://doi.org/10.1038/s41598-019-42646-4

Molan, P.C., 1992. The antibacterial activity of honey. Bee World, 73, 59–76. DOI: https://doi.org/10.1080/0005772X.1992.11099118

Olaitan, P.B., Adeleke, O.E., Iyabo, O.O., 2007. Honey: a reservoir for microorganisms and an inhibitory agent for microbes. African Health Sciences, 7, 159–165.

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: https://doi.org/10.1016/j.jtv.2015.12.002

Panatto, D., Gasparini, R., Lai, P., Rovatti, P., Gallelli, G., 2007. Long-term decline of 137Cs concentra- tion in honey in the second decade after the Chernobyl accident. Science of the Total Environment, 382, 147–152. DOI: https://doi.org/10.1016/j.scitotenv.2007.03.040

Perko, D., 1998. The regionalization of Slovenia. Acta Geographica, 38, 11–57.

Podrižnik, B., Božič, J., 2015. Maturation and stratification of antibacterial activity and total phenolic content of bee bread in honey comb cells. Journal of Apicultural Research, 54, 81–92. DOI: https://doi.org/10.1080/00218839.2015.1090774

Poormasjedi-Meibod, M.-S., Hartwell, R., Kilani, R.T., Ghahary, A., 2014. Anti-scarring properties of different tryptophan derivatives. PLOS ONE 9, e91955. DOI: https://doi.org/10.1371/journal.pone.0091955

Ramanathan, A.N.K.G., Nair, A.J., Sugunan, V.S., 2018. A review on royal jelly proteins and peptides. Journal of Functional Foods, 44, 255–264. DOI: https://doi.org/10.1016/j.jff.2018.03.008

Saitta, M., Bella, G.D., Fede, M.R., Turco, V.L., Potortì, A.G., Rando, R., Russo, M.T., Dugo, G., 2017. Gas chromatography-tandem mass spectrometry multi-residual analysis of contaminants in Italian honey samples. Food Additives & Contaminants: Part A, 34, 800–808. DOI: https://doi.org/10.1080/19440049.2017.1292054

Silva, M.S., Rabadzhiev, Y., Eller, M.R., Iliev, I., Ivanova, I., Santana, W.C., 2017. Microorganisms in honey. Honey Analysis. DOI: https://doi.org/10.5772/67262

Snowdon, J.A., Cliver, D.O., 1996. Microorganisms in honey. International Journal of Food Micro- biology, 31, 1–26. DOI: https://doi.org/10.1016/0168-1605(96)00970-1

Sojka, M., Valachova, I., Bucekova, M., Majtan, J., 2016. Antibiofilm efficacy of honey and bee-derived defensin-1 on multispecies wound biofilm. Journal of Medical Microbiology, 65, 337–344. DOI: https://doi.org/10.1099/jmm.0.000227

Szweda, P., 2017. Antimicrobial activity of honey. Honey Analysis, 1, 215–232. DOI: https://doi.org/10.5772/67117

Takenaka, T., Ito, H., Yatsunami, K., Echigo, T., 1990. Changes of glucose oxidase activity and amount of gluconic acid formation in the hypopharyngeal glands during the lifespan of honey bee workers (Apis mellifera L.). Agricultural and Biological Chemistry, 54, 2133–2134. DOI: https://doi.org/10.1271/bbb1961.54.2133

Tian, W., Li, M., Guo, H., Peng, W., Xue, X., Hu, Y., Liu, Y., Zhao, Y., Fang, X., Wang, K., Li, X., Tong, Y., Conlon, M.A., Wu, W., Ren, F., Chen, Z., 2018. Architecture of the native major royal jelly protein 1 oligomer. Nature Communications, 9, 3373. DOI: https://doi.org/10.1038/s41467-018-05619-1

Truchado, P., Gil-Izquierdo, A., Tomás-Barberán, F., Allende, A., 2009a. Inhibition by chestnut honey of N-Acyl-l-homoserine lactones and biofilm formation in Erwinia carotovora, Yersinia enteroco- litica and Aeromonas hydrophila. Journal of Agricultural and Food Chemistry, 57, 11186–11193. DOI: https://doi.org/10.1021/jf9029139

Truchado, P., López-Gálvez, F., Gil, M.I., Tomás-Barberán, F.A., Allende, A., 2009b. Quorum sensing inhibitory and antimicrobial activities of honeys and the relationship with individual phenolics. Food Chemistry, 115, 1337–1344. DOI: https://doi.org/10.1016/j.foodchem.2009.01.065

Truchado, P., Martos, I., Bortolotti, L., Sabatini, A.G., Ferreres, F., Tomas-Barberan, F.A., 2009c. Use of quinoline alkaloids as markers of the floral origin of chestnut honey. Journal of Agricultural and Food Chemistry, 57, 5680–5686. DOI: https://doi.org/10.1021/jf900766v

Turski, M.P., Chwil, S., Turska, M., Chwil, M., Kocki, T., Rajtar, G., Parada-Turska, J., 2016. An exceptionally high content of kynurenic acid in chestnut honey and flowers of chestnut tree. Journal of Food Composition and Analysis, 48, 67–72. DOI: https://doi.org/10.1016/j.jfca.2016.02.003

Wiest, L., Buleté, A., Giroud, B., Fratta, C., Amic, S., Lambert, O., Pouliquen, H., Arnaudguilhem, C., 2011. Multi-residue analysis of 80 environmental contaminants in honeys, honeybees and pollens by one extraction procedure followed by liquid and gas chromatography coupled with mass spec- trometric detection. Journal of Chromatography A, 1218, 5743–5756. DOI: https://doi.org/10.1016/j.chroma.2011.06.079

Winston, M.L., 1991. The biology of the honey bee. Harvard University Press.

Downloads

Published

01.12.2020

Issue

Section

Original Research Paper

How to Cite

Božič, J., Bertoncelj, J., Drobne, D., Glavan, G., Gunde Cimerman, N., Leonardi, A., Kopinč, R., Jemec Kokalj, A., Novak, S., Korošec, M., Križaj, I., Podrižnik, B., Turk, M., & Zabret, A. (2020). The quality of Slovenian chestnut honey and its specific properties relevant for medical application and functional nutrition. Acta Biologica Slovenica, 63(2), 31-44. https://doi.org/10.14720/abs.63.2.15935

Similar Articles

1-10 of 57

You may also start an advanced similarity search for this article.

Most read articles by the same author(s)

1 2 > >>