Influence of Botanical Origin and Chemical Composition on the Protective Effect against Oxidative Damage and the Capacity to Reduce In Vitro Bacterial Biofilms of Monofloral Honeys from the Andean Region of Ecuador

International Journal of Molecular Sciences - Tập 19 Số 1 - Trang 45
Marilyn García-Tenesaca1, Eillen S. Navarrete1, GABRIEL A. ITURRALDE2, Irina Villacrés‐Granda2, Eduardo Tejera3, Pablo Beltrán-Ayala4, Francesca Giampieri5, Maurizio Battino5, José M. Álvarez-Suárez6
1Facultad de Ingeniería y Ciencias Agropecuarias, Universidad de Las Américas, Quito 170125, Ecuador
2Laboratorios de Investigación, Universidad de Las Américas, Quito 170125, Ecuador
3Facultad de Ingeniería y Ciencias Agropecuarias, Grupo de Bioquimioinformática, Universidad de Las Américas, Quito 170125, Ecuador
4Colegio de Administración y Economía, Universidad San Francisco de Quito, Cumbayá, Quito 170157, Ecuador
5Dipartimento di Scienze Cliniche Specialistiche ed Odontostomatologiche (DISCO)-Sez. Biochimica, Facolta di Medicina, Università Politecnica delle Marche, 60121 Ancona, Italy
6Escuela de Medicina Veterinaria y Zootecnia, Grupo de Investigación en Biotecnología Aplicada a Biomedicina (BIOMED), Universidad de Las Américas, Quito 170125, Ecuador

Tóm tắt

Three types of monofloral honey from the Andean regions of Ecuador (Avocado, Eucalyptus, and Rapeseed honey) were analyzed to determine their floral origin, physicochemical parameters, chemical composition, antioxidant capacity, and their capacity to reduce in vitro bacterial biofilms. The chemical composition varied considerably depending on floral origin. The highest values of bioactive compounds were found in Avocado honey, classified as dark amber in color, while the lowest values were found in Eucalyptus honey followed by Rapeseed honey, both classified as extra light amber. When compared to Eucalyptus and Rapeseed honey, Avocado honey showed a more effective superoxide scavenging activity, chelating metal ions capacity, and a higher ability to protect human erythrocyte membranes against lipid peroxidation. For antimicrobial activity, the hydrogen peroxide content and the capacity to inhibit the biofilm formation, and to remove preformed biofilm from Staphylococcus aureus and Klebsiella pneumoniae was determined. Avocado honey showed the highest values of hydrogen peroxide content, as well as the highest capacity to reduce in vitro bacterial biofilms. A correlation between color vs. phenolics content vs. superoxide scavenging activity vs. chelating metal ions capacity, and the capacity to protect human erythrocyte membranes against lipid peroxidation was found.

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Tài liệu tham khảo

Giampieri, 2016, Activation of AMPK/Nrf2 signalling by Manuka honey protects human dermal fibroblasts against oxidative damage by improving antioxidant response and mitochondrial function promoting wound healing, J. Funct. Foods, 25, 38, 10.1016/j.jff.2016.05.008

Giampieri, 2013, Honey as a source of dietary antioxidants: Structures, bioavailability and evidence of protective effects against human chronic diseases, Curr. Med. Chem., 20, 621, 10.2174/092986713804999358

Cooper, 2016, Honey for wound care in the 21st century, J. Wound Care, 25, 544, 10.12968/jowc.2016.25.9.544

Alvarez-Suarez, J.M. (2017). Honey Health Benefits and Uses in Medicine. Bee Products—Chemical and Biological Properties, Springer International Publishing.

Alvarez-Suarez, J.M. (2017). Chemical Composition of Honey. Bee Products—Chemical and Biological Properties, Springer International Publishing.

Acquarone, 2007, Pattern of pH and electrical conductivity upon honey dilution as a complementary tool for discriminating geographical origin of honeys, Food Chem., 101, 695, 10.1016/j.foodchem.2006.01.058

2014, Physicochemical characteristics of minor monofloral honeys from Tenerife, Spain, LWT—Food Sci. Technol., 55, 572, 10.1016/j.lwt.2013.09.024

Terrab, 2005, Multivariate correlation between color and mineral composition of honeys and by their botanical origin, J. Agric. Food Chem., 53, 2574, 10.1021/jf048207p

Flores, 2014, Characterization of Eucalyptus globulus honeys produced in the eurosiberian area of the Iberian Peninsula, Int. J. Food Prop., 17, 2177, 10.1080/10942912.2013.790050

Piro, 2004, Main European unifloral honeys: Descriptive sheets, Apidologie, 35, S38, 10.1051/apido:2004049

Stawiarz, 2008, Pollen spectrum of rapeseed honey from the sandomierska upland area, J. Apic. Sci., 52, 83

Florek, 2016, Effect of freezing and room temperatures storage for 18 months on quality of raw rapeseed honey (Brassica napus), J. Food Sci. Technol., 53, 3349, 10.1007/s13197-016-2313-x

(2002). EU Council, Council directive 2001/11 O/EC of 20 December 2001 relating to honey. Off. J. Eur. Commun., 10, 47–52.

Chirife, 2006, The correlation between water activity and % moisture in honey: Fundamental aspects and application to Argentine honeys, J. Food Eng., 72, 287, 10.1016/j.jfoodeng.2004.12.009

Terrab, 2004, Characterization of avocado (Persea americana Mill) honeys by their physicochemical characteristics, J. Sci. Food Agric., 84, 1801, 10.1002/jsfa.1888

2016, Physicochemical characteristics of commercial eucalyptus honeys from Southwest Casanare, Corpoica Cienc. Tecnol. Agropecu., 17, 73

Fallico, 2006, The European Food Legislation and its impact on honey sector, Accred. Qual. Assur., 11, 49, 10.1007/s00769-006-0128-6

Tulipani, 2010, Antioxidant and antimicrobial capacity of several monofloral Cuban honeys and their correlation with color, polyphenol content and other chemical compounds, Food Chem. Toxicol., 48, 2490, 10.1016/j.fct.2010.06.021

Gauche, 2016, Honey: Chemical composition, stability and authenticity, Food Chem., 196, 309, 10.1016/j.foodchem.2015.09.051

Ramos, 2018, Effect of botanical and physicochemical composition of Argentinean honeys on the inhibitory action against food pathogens, LWT—Food Sci. Technol., 87, 457, 10.1016/j.lwt.2017.09.014

Cooper, 2002, The sensitivity to honey of Gram-positive cocci of clinical significance isolated from wounds, J. Appl. Microbiol., 93, 857, 10.1046/j.1365-2672.2002.01761.x

Pastor, 2013, Comparative analysis of antioxidant activity of honey of different floral sources using recently developed polarographic and various spectrophotometric assays, J. Food Comp. Anal., 30, 13, 10.1016/j.jfca.2012.12.004

Giampieri, 2012, Radical-scavenging activity, protective effect against lipid peroxidation and mineral contents of monofloral cuban honeys, Plant Foods Hum. Nutr., 67, 31, 10.1007/s11130-011-0268-7

Henriques, 2006, Free radical production and quenching in honeys with wound healing potential, J. Antimicrob. Chemother., 58, 773, 10.1093/jac/dkl336

Vit, 2006, Antioxidant capacity of Venezuelan honey in wistar rat homogenates, J. Med. Food, 9, 510, 10.1089/jmf.2006.9.510

Visioli, 2012, Polyphenols and health: Moving beyond antioxidants, J. Berry Res., 2, 63, 10.3233/JBR-2012-028

Niki, 2011, Antioxidant capacity: Which capacity and how to assess it?, J. Berry Res., 1, 169, 10.3233/JBR-2011-018

Morita, 2017, Antioxidant capacity of blueberry extracts: Peroxyl radical scavenging and inhibition of plasma lipid oxidation induced by multiple oxidants, J. Berry Res., 7, 1, 10.3233/JBR-170152

Ferreira, 2009, Antioxidant activity of Portuguese honey samples: Different contributions of the entire honey and phenolic extract, Food Chem., 114, 1438, 10.1016/j.foodchem.2008.11.028

Gomes, 2010, Physicochemical, microbiological and antimicrobial properties of commercial honeys from Portugal, Food Chem. Toxicol., 48, 544, 10.1016/j.fct.2009.11.029

Cokcetin, N.N., Pappalardo, M., Campbell, L.T., Brooks, P., Carter, D.A., Blair, S.E., and Harry, E.J. (2016). The antibacterial activity of Australian Leptospermum honey correlates with methylglyoxal levels. PLoS ONE, 11.

Giampieri, 2018, Apis mellifera vs. Melipona beecheii Cuban polifloral honeys: A comparison based on their physicochemical parameters, chemical composition and biological properties, LWT—Food Sci. Technol., 87, 272, 10.1016/j.lwt.2017.08.079

Stramm, 2013, Comparative study of the physicochemical and palynological characteristics of honey from Melipona subnitida and Apis mellifera, Int. J. Food Sci. Technol., 48, 1698, 10.1111/ijfs.12140

Kwakman, 2012, Antibacterial components of honey, IUBMB Life, 64, 48, 10.1002/iub.578

Gauhe, 1940, Über ein glukoseoxydierendes Enzym in der Pharynxdrüse der Honigbiene, Z. Vgl. Physiol., 28, 211, 10.1007/BF00342436

Alaux, 2010, Diet effects on honeybee immunocompetence, Biol. Lett., 6, 562, 10.1098/rsbl.2009.0986

Weston, 2000, The contribution of catalase and other natural products to the antibacterial activity of honey: A review, Food Chem., 71, 235, 10.1016/S0308-8146(00)00162-X

Li, 2017, A modified FOX-1 method for Micro-determination of hydrogen peroxide in honey samples, Food Chem., 237, 225, 10.1016/j.foodchem.2017.05.065

Lu, 2014, Manuka-type honeys can eradicate biofilms produced by Staphylococcus aureus strains with different biofilm-forming abilities, PeerJ, 2, e326, 10.7717/peerj.326

Majtan, 2014, Anti-biofilm effects of honey against wound pathogens Proteus mirabilis and Enterobacter cloacae, Phytother. Res., 28, 69, 10.1002/ptr.4957

Jagani, 2009, Effects of phenol and natural phenolic compounds on biofilm formation by Pseudomonas aeruginosa, Biofouling, 25, 321, 10.1080/08927010802660854

Louveaux, 1978, Methods of Melissopalynology, Bee World, 59, 139, 10.1080/0005772X.1978.11097714

Piana, 2004, Harmonized methods of melissopalynology, Apidologie, 35, 18, 10.1051/apido:2004050

IHC (2002). Harmonised Methods of the International Honey Commission, Swiss Bee Research Centre.

Singleton, 1999, Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent, Methods Enzymol., 299, 152, 10.1016/S0076-6879(99)99017-1

Chang, 2002, Estimation of total flavonoid content in propolis by two complementary colorimetric methods, J. Food Drug Anal., 10, 178

Doi, 1981, Modified colorimetric ninhydrin methods for peptidase assay, Anal. Biochem., 118, 173, 10.1016/0003-2697(81)90175-5

Benzie, 1996, The Ferric Reducing Ability of Plasma (FRAP) as a measure of “Antioxidant Power”: The FRAP Assay, Anal Biochem., 239, 70, 10.1006/abio.1996.0292

Tournier, 2003, Antioxidant activity of Paraguayan plant extracts, Fitoterapia, 74, 91, 10.1016/S0367-326X(02)00293-9

Wang, 2004, Supercritical fluid extractive fractionation—Study of the antioxidant activities of propolis, Food Chem., 86, 237, 10.1016/j.foodchem.2003.09.031

Oyanagui, 1984, Reevaluation of assay methods and establishment of kit for superoxide dismutase activity, Anal. Biochem., 142, 290, 10.1016/0003-2697(84)90467-6

Giampieri, 2012, Phenolics from monofloral honeys protect human erythrocyte membranes against oxidative damage, Food Chem. Toxicol., 50, 1508, 10.1016/j.fct.2012.01.042

Lowry, 1951, Protein measurement with the Folin phenol reagent, J. Biol. Chem., 193, 265, 10.1016/S0021-9258(19)52451-6

Buege, 1978, Microsomal lipid peroxidation, Methods Enzymol., 52, 302, 10.1016/S0076-6879(78)52032-6