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  • a Department of Chemistry, Karadeniz Technical University, Trabzon, Turkey
  • | b Department of Food Engineering, Tekirdağ Namık Kemal University, Tekirdağ, Turkey
  • | c Vocational School of Health Services, Bilecik Şeyh Edebali University, Bilecik, Turkey
  • | d Department of Biology, Recep Tayyip Erdoğan University, Rize, Turkey
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Honey is the most important bee product. There are many secondary metabolites, carbohydrates, enzymes, and vitamins in honey, thus, honey has antimicrobial activity. In this study, in vitro antimicrobial activity of forty-two honey and eight propolis ethanolic extracts (PEE) were investigated against 16 microorganisms. Total phenolic content ranged between 20.00–124.10 mg GAE/100 g and 103–232 mg GAE/g for honey and raw propolis samples, respectively. Pine and oak honeydew honeys had higher antimicrobial activity than four different grades of Manuka Honeys up to 18 mm minimum inhibition zone diameters. The ethanolic propolis extracts showed much higher antimicrobial activity than the honey samples. Fungi species were inhibited by the propolis samples. Helicobacter pylorii (H. pylorii) was the most sensitive, whereas Streptococcus agalactiae was the most resistant bacteria among the studied microorganisms. Brazilian and Zonguldak propolis had the closest antimicrobial activity to ampicillin, streptomycin, and fluconazole. It can be concluded that both honey and propolis could be used in preservative and complementary medicine.

Abstract

Honey is the most important bee product. There are many secondary metabolites, carbohydrates, enzymes, and vitamins in honey, thus, honey has antimicrobial activity. In this study, in vitro antimicrobial activity of forty-two honey and eight propolis ethanolic extracts (PEE) were investigated against 16 microorganisms. Total phenolic content ranged between 20.00–124.10 mg GAE/100 g and 103–232 mg GAE/g for honey and raw propolis samples, respectively. Pine and oak honeydew honeys had higher antimicrobial activity than four different grades of Manuka Honeys up to 18 mm minimum inhibition zone diameters. The ethanolic propolis extracts showed much higher antimicrobial activity than the honey samples. Fungi species were inhibited by the propolis samples. Helicobacter pylorii (H. pylorii) was the most sensitive, whereas Streptococcus agalactiae was the most resistant bacteria among the studied microorganisms. Brazilian and Zonguldak propolis had the closest antimicrobial activity to ampicillin, streptomycin, and fluconazole. It can be concluded that both honey and propolis could be used in preservative and complementary medicine.

Honey and propolis are important apitherapic agents, and they have many different biological activities, such as antimicrobial, antioxidant, anti-inflammatory, immune-modulator, anti- tumor, etc. (Amuja & Amuja, 2010; Can et al., 2015; Pobieua et al., 2019). Honey consists of carbohydrates (65–75%), moisture (15–20%), minerals, and various secondary metabolites (1–2%) (Can et al., 2015). The four main reasons explaining why honey is a good antimicrobial agent are: its pH, viscosity, hydrogen peroxide source from glucose oxidase, and secondary metabolites (Kolayli et al., 2016). Except secondary metabolites, the other three substances are common in all honey samples. The amount, variety, and kind of the secondary metabolite differ according to honey types (Amuja & Amuja, 2010). Raw propolis is composed mainly of resin (40–50%), wax (25–30%), essential compounds (5–10%), pollens (2–5%), and numerous other organic molecules (polyphenols, vitamins, and sugars) (Keskin & Kolayli, 2018). It was noted that propolis is one of the best pharmaceutical agents, and it contains many different bioactive compounds. The number of flavonoids and its phenyl esters were present in the extracts with antibacterial effects on pathological microorganisms. In this study, antimicrobial and antifungal effects of 42 different honey and eight propolis samples were compared.

1 Materials and methods

1.1 Samples collections and test microorganisms

In this study, 42 different honey samples were investigated. Honey samples were mostly collected from Turkey in 2016–2017 harvest seasons, and some of them were obtained from different countries as shown in Table 1. Four different grades of Unique Manuka Factor (UMF) certificated Manuka honey samples (UMF-10+, UMF12+, UMF15+, and UMF20+) were purchased from The Real Honey Company, England. Propolis samples were collected from different regions of Turkey. Brazilian Red propolis (raw) was purchased from a Brazilian company, Natura Nectar. All test microorganisms were obtained from the Hıfzıssıhha Institute of Refik Saydam (Ankara, Turkey). Thirteen bacterial strains and 3 fungal strains (Ec : Escherichia coli ATCC 25922; Yp: Yersinia pseudotuberculosis ATCC 911; Kp: Klebsiella pneumonia subp. pneumonia ATCC18883; Pa: Pseudomonas aeruginosa ATCC 27853; Hp: Helicobacter pyloriii J99; Sa: Staphylococcus aureus ATCC 25923; Ef: Enterococcus faecalis ATCC 29212; Sm: Streptococcus mutans RSKK07038; Sag: Streptococcus agalactiae (clinic strain); Bc: Bacillus cereus 702 Roma; La: Lactobacillus acidophilus RSKK06029; Lc: Lactobacillus casei RSKK591; Ms: Mycobacterium smegmatis ATCC607; Ca: Candida albicans ATCC 60193; Ct: Candida tropicalis ATCC 13803; Sc: Saccharomyces cerevisiae) used in the current study were clinical isolates obtained from RTE University’s Hospitals, Rize.

Table 1

Specifications of studied honey and propolis samples

Sample nameSample codeSample typesRegionDominant pollensProperties
ManukaH1Manuka UMF +10New ZealandL. scopariumCommercial
H2Manuka UMF +12L. scopariumCommercial
H3Manuka UMF +15L. scopariumCommercial
H4Manuka UMF +20L. scopariumCommercial
UnifloralH5SunflowerKırklareli/Helianthus annuusTurkey
honeysH6SunflowerTekirdagHelianthus annuus
H7ChestnutOrduCastanea sativa
H8ChestnutKureCastanea sativa
H9AstragalusPalandökenAstragalus microcephalus
H10AstragalusErzurumAstragalus microcephalus
H11ThymeÇanakkaleThymus vulgaris
H12R.caucasiumRizeRhododendron
H13R.ponticumTrabzonRhododendron
H14PumpkinIzmirPumpkin
H15Cultivated ThymeDenizliThymus vulgaris
H16Natural ThymeDenizliThymus vulgaris
H17CalltropBursaEryngium campestre
H18ThistleHataySilybium marianum
H19CorianderBurdurCoriandrum sativum
H20HarnupHatayCeratonia siliqua
H21Black CuminAdanaNigella sativa
H22NettleorurticaUskupUrtica dioicaMacadonia
H23HeatherMuglaCalluna vulgarisTurkey
H24HeatherMuglaCalluna vulgaris
H25BuckwheatKonyaFagopyrum esculentum
H26BuckwheatSamsunFagopyrum esculentum
H27GorseKırklareliPaliurus aculeatus
H28CedarHailCedrus ssp.Saudi Arabia
H29AcaciaThomtreeTaifAcacia ssp.
H30TalhaThomtreeTalha tree
H31Ivy, HederaKırklareliHedera helixTurkey
HoneyH32HoneydewRizeForest honeyTurkey
dewH33HoneydewGümüşhaneForest honey
H34HoneydewArsinForest honey
H35OakKırklareliOak spp.
H36OakSamsunOak spp.
H37PineMuğlaPinus L.
H38PineIzmirPinus L.
Multi-H39BlossomAnzerPlateau honey
floralH40BlossomGümüşhanePlateau honey
H41BlossomHakkariPlateau honey
H42BlossomHakkariPlateau honey
Raw PropolisP1 P2Red Brazilian KarsBrezillia TurkeyBrazilia Turkey
P3YığılcaTurkey
P4ZonguldakTurkey
P5AnkaraTurkey
P6ErzurumTurkey
P7KonyaTurkey
P8ArtvinTurkey

1.2 Honey classifications, propolis extraction, and determination of total phenolic content

The honey and propolis samples were obtained from different regions that have different botanical origin (Table 1). The honey samples were classified according to Santiauo and co-workers (2018). The propolis extracts were prapered according to Keskin and Kolayli (2018). Total phenolic compounds of the samples were determined using the Folin-Ciocalteu spectrophotometric assay (Sinuleton et al., 1999).

1.3 Agar well diffusion method

Simple susceptibility screening method was used by employing the agar-well diffusion method (Woods et al., 2003).

1.4 Statistical analysis

The analyses were performed three times, the results were presented as mean values and standard deviations. Regression analysis of the data was performed in Microsoft Office Excel 2013 (Microsoft Corporation, Redmond, WA, USA).

2 Results and discussion

Total phenolic content of honey and propolis samples depends on geographical origin (Keskin et al., 2020). In a study, it is reported that total amount of phenolic content of Anatolian raw propolis varies between 16.13–178.34 mg GA/g (Keskin & Kolayli, 2018) and total amount of phenolic content of honey samples ranged between 33 mg GA/100 g and 81 mg GA/100 g (Keskin et al., 2020). It is clear from the obtained results that the unifloral and honeydew honey samples had higher phenolic compounds than multifloral honeys (Table 2). Although the honey samples showed different inhibition effects against the 16 microorganisms, the honey samples mostly affected E. coli, Y. pseudotuberculosis, K. pneumonia, S. aureus, and M. smegmatis (Table 3). P. aeruginosa, S. mutans, L. casei, and yeast like fungus of C. albicans, C. tropicalis, and S. cerevisiae were not affected by any of the honey samples. At the beginning of the study, Manuka honeys were used as positive controls, because numerous investigations in the literature show that these honeys have high antimicrobial activities. Surprisingly, only 4 microorganisms, Y. pseudotuberculosis, K. pneumonia, S. aureus, and M. smegmatis, were inhibited by the Manuka honey samples. Although Manuka UMF +10 and +12 samples had moderate antimicrobial effects on H. pylorii (8 and 10 mm, respectively), heather honey from Muğla region had better activity against these bacteria (12–15 mm). Moreover, there were no substantial antimicrobial differences among the four Manuka honeys. Among the honey samples, H11-15, H17-19, H21-23, H25-26, H31-32, and H34-36 showed the highest inhibitions against S. aureus (Table 3). Although honey samples generally showed inhibition effects against M. smegmatis, cedar, acacia, and Talha (H28, H29, and H30) honey samples obtained from Saudi Arabia were the most effective honey samples against this microorganism. The three unifloral honeys of cedar (H28), acacia (H29), and Talha (H41) were found to be very effective especially against Lactobacillus acidophilus, L. casei, and M. smegmatis. Some bacteria (L. acidophilus,L. casei, and S. aureus) are related to dental health and tooth decay (Yadav & Prakasm, 2017), and the inhibition of these bacteria by honeys is an important finding. In general, there were no major differences found between the honey samples against the four bacteria (Y. pseudotuberculosis, K. pneumonia, S. aureus, and M. smegmatis). Different authenticities of the honeys have also showed dissimilar inhibitions among the 16 microorganisms (Table 3).

Table 2

Total phenolic content of honey and propolis samples

SampleTotal phenolic content mg GAE/100 gSampleTotal phenolic content mg GAE/100 gSampleTotal phenolic content mg GAE/100 gSampleTotal phenolic content mg GAE/100 gSampleTotal phenolic content mg GAE/g
H158.11±0.31H1235.33±1.55H2364.41±2.30H3461.60±1.33P1232.10± 5.20
H256.43±0.46H1342.80±2.30H2468.05±2.08H3574.20±2.10P2146.30± 1.20
H345.78±0.49H1428.60±0.87H2552.40±1.04H3663.06±1.66P3174.50±3.56
H449.27±0.31H1552.22±2.30H2646.32±3.02H3748.44±1.40P4162.22±2.55
H528.20±2.20H1660.03±3.70H2737.04±1.04H3842.20±0.80P5106.56±1.15
H631.05±1.30H1735.63±1.44H28105.10±4.20H3935.38±0.58P6110.45±2.14
H758.02±3.20H1825.88±0.62H2998.20±2.10H4028.52±0.60P7103.30±0.41
H865.20±2.05H1947.40±2.01H30124.05±2.30H4124.20±0.41P8132.74 ±0.36
H935.40±1.08H2020.02±0.35H3135.20±1.22H4226.39±1.04
H1037.10±0.98H2156.05±0.74H3264.07±3.02
H1157.50±2.33H2224.32±0.43H3353.36±2.00
Table 3

Antimicrobial activities of honey samples against a range of microorganisms

SamplesCodeTested microorganisms and minimum inhibition zone diameters (mm)
Gram negative bacteriaGram positive bacteriaOther Yeast like fungi
EcYpKpPaHpSaEfSmSagBcLaLcMsCaCtSc
ManukaH186886
H2661086
H36686
H48888
UnifloralH5888668
honeysH66610668
H788610610
H881081010
H961081066
H1061081066
H11681466
H12668156
H138681666
H146156
H156810141086
UnifloralH1668812868
honeysH1768161212126
H186101666
H1966815688
H20666
H21810186610
H2266166
H2386615186
H2410121011
H25881082010121012
H26101010101610101010
H27661286
H286108108151515
H2981261010108203030
H30810101010118203015
H31812814141014
HoneydewH321010101661012
H338888101010
H34671016661010
H3512168810156810810
H36101468818888
H371268128
H381068108
MulifloralH398868108
H401061010106
H416668101588666
H4268106

Ec: Escherichia coli ATCC 25922, Yp: Yersinia pseudotuberculosis ATCC 911, Kp: Klebsiella pneumonia subsp. pneumonia ATCC18883, Pa: Pseudomonas aeruginosa ATCC 27853, Hp: Helicobacter pylorii J99, Sa: Staphylococcus aureus ATCC 25923, Ef: Enterococcus faecalis ATCC 29212, Sm: Streptococcus mutans RSKK07038, Sag: Streptococcus agalactiae (clinical strain), Bc: Bacillus cereus 702 Roma, La: Lactobacillus acidophilus RSKK06029, Lc: Lactobacillus casei RSKK591, Ms: Mycobacterium smegmatis ATCC607, Ca: Candida albicans ATCC 60193, Ct: C. tropicalis ATCC 13803, Sc: Saccharomyces cerevisiae RSKK 251, (—): No activity. 6–9 mm; low activity, 9–11 mm; moderate activity, ≥12; good activity

Table 4

Antimicrobial activities of the ethanolic propolis samples against a range of microorganisms

Propolis samplesTested microorganisms and inhibition zone diameters (mm)

Gram negative bacteriaGram positive bacteriaOtherYeast like fungi
EcYpKpPaHpSaEfSmSagBcLaLcMsCaCtSc
P18151112452220121218241220161420
P2810824401886612146151468
P310812502012101014251218121220
P4121010184520151212122214251412
P5861484010156615156186610
P61010121045141066141881715815
P71210610401615101014181015151214
P8886184016101088181012108
Amp.10101018NT3510NTNT15NTNT
Strep.35
Flu.252525

Ec: Escherichia coli ATCC 25922; Yp: Yersinia pseudotuberculosis ATCC 911; Kp: Klebsiella pneumonia subsp. pneumonia ATCC18883; Pa: Pseudomonas aeruginosa ATCC 27853; Hp: Helicobacter pyloriii J99; Sa: Staphylococcus aureus ATCC 25923; Ef: Enterococcus faecalis ATCC 29212; Sm: Streptococcus mutans RSKK07038; Sag: Streptococcus agalactiae (clinical strain); Bc: Bacillus cereus 702 Roma; La: Lactobacillus acidophilus RSKK06029; Lc: Lactobacillus casei RSKK591; Ms: Mycobacterium smegmatis ATCC607; Ca: Candida albicans ATCC 60193; Ct: C. tropicalis ATCC 13803; Sc: Saccharomyces cerevisiae RSKK 251; (—): No activity. 6–9 mm; low activity; 9–11 mm; moderate activity; ≥12; good activity

For example, only Arabian honeys (H28, H29, and H30) and multifloral honey from Hakkari (H41) showed moderate inhibition against S. mutans. In addition, only two buckwheat honeys showed moderate inhibition against C. albicans and C. tropicalis. At the same time, only the buckwheat honeys and the oak honeys showed moderate inhibition against S. cerevisiae. Nearly half of the honey samples showed a weak inhibition against L. acidophilus, while the S. Arabic region honeys showed high inhibition effects. Saudi Arabian honeys had the highest phenolic contents (Table 2), and oak, chestnut, heather, buckwheat, and Manuka honeys had higher total phenolic contents than multifloral and blossom honeys. It was reported earlier that oak, chestnut, and heather honeys were dark colored honeys and contained higher phenolic compounds (Can et al., 2015). Cedar, black cumin (Nigella sativa), and Manuka honeys showed a good bactericidal-bacteriostatic inhibition effect against only Staphylococcus aureus (Almasaudi et al., 2017), and our results supported these findings. Antimicrobial activity of honey samples could be due to the quantity and synergistic effect of key phenolics (Kaloueropoulos et al., 2009). The antimicrobial activities of the propolis extracts are given in Table 3. All propolis samples showed inhibition against the studied microorganisms to diferent extent, but the widest inhibition zone was found againts H. pylori, which is a fastidious, Gram negative bacterium that grows poorly in broth culture. Our findings showed that propolis extracts have much better inhibition effects than honey samples, which clearly shows that propolis is a much better antimicrobial agent than honey. All samples had the highest antimicrobial activity against H. pylori, with Yıgılca (P3) propolis showing the best results. In a previous study, gastric system bacteria were found sensitive to many different Anatolia propolis samples, the inhibition zone diameters ranged from 18 to 22 mm (Velikova et al., 2000). Moreover, in the same study, the anti-urease activity of Anatolia propolis was studied, and the ethanolic extracts showed a good inhibition of the extracellular urease of the bacteria. It was reported that these bee products, either honey or propolis, killed bacteria by inhibition of their urease enzyme (Baltas et al., 2016). It was notably seen that all studied propolis samples showed good antimicrobial activity against Gram negative bacteria. In the previous studies, poplar type propolis samples were found ineffective and Bulgarian type was effective against E.coli (Velikova et al., 2000). The good activity found in this study can be due to similar constituents found in Bulgarian and Turkish propolis (Velikova et al., 2000). In this study, the highest total phenolic content in propolis was found in the Brazilian sample, showing a good inhibition against all bacteria and fungi to different extent. Some bacteria are even affected by low doses of propolis, while others need high doses. These findings are also confirmed by other studies (Neto et al., 2017). The propolis samples were also found very effective against oral pathogens such as Streptococcus mutans, Enterococcus faecalis, and C. albicans. Propolis samples have higher antimicrobial activity than honey samples, and the antimicrobial activity of propolis samples depend on their total phenolic content. Therefore, according to typification approach in the standardisation process, similar plant sources should be investigated for Brazilian and Turkish propolis to determine key chemicals providing the antimicrobial effect.

3 Conclusions

Honey and propolis are substantial antibacterial and antifungal agents, and their antimicrobial effects could result from their floral sources, but antimicrobial activities were found not to be dependent on their total phenolic contents. For this reason, further studies are needed to evaluate those mechanisms. Better antimicrobial effects of propolis implied that wherever they live, bees are created to sense, find, and collect the best chemicals in any environment to protect their hives against microorganisms. Therefore, this natural product could be used in preservative and complementary medicine.

Funding: This study was supported by TUBITAK [grant number 114Z370].

  • Amuja, A. & Amuja, V. (2010): Apitherapy–A sweet approach to dental diseases. Part I: Honey. J. Adv. Dental Res., 1, 8186.

  • Almasaudi, S.B., Al Namari, A.A., El Sayed, M., Barbour, E., Al Mumayayi, S. M., & Harakem, S. (2017): Antimicrobial effect of different types of honey on Staphylococcus aureus. Saudi J. Biol. Sci., 24(6), 12551261.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Baltas, N., Yildiz, O. & Kolayli, S. (2016): Inhibition properties of propolis extracts to some clinically important enzymes. J. Enzyme Inhib. Med. Ch., 31, 5255.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Can, Z., Yildiz, O., Şamin, H., Asadov, A. & Kolayli, S. (2015): Phenolic profile and antioxidant potential of propolis from Azerbaijan. Mellifera, 15(1), 1628.

    • Search Google Scholar
    • Export Citation
  • Kaloueropoulos, N., Konteles, S.J., Troullidou, E., Mourtzinos, I. & Karatmanos, V.T. (2009): Chemical composition, antioxidant activity and antimicrobial properties of propolis extracts from Greece and Cyprus. Food Chem., 116(2), 452461.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Keskin, M. & Kolayli, S. (2018): Standardization of propolis, is it possible? Uludag Bee J., 18(2),101110.

  • Keskin, Ş., Mayda, N., Keskin, M. & Özkök, A. (2020): Investigation of Bilecik honeys in terms of melissopalynology and chemical analyses. GIDA–J. Food, 45(2), 275289.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kolayli, S., Cakir, H.E. & Samin, H. (2016): Anti-inflammatory activities of some bee products by inhibition of bovine testes hyaluronidase. Curr. Enzyme Inhib., 12(2), 183187.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Neto, M.R., Tintino, S.R., Da Silva, A.R.P., Do Socorro Costa, M., Boliuon, A.A., & Coutinmo, H.D.M. (2017): Seasonal variation of Brazilian red propolis: Antibacterial activity, synergistic effect and phytochemical screening. Food Chem. Toxicol., 107, 572580

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Pobieua, K., Kra¿nieyska, K. & Gnieyosz, M. (2019): Application of propolis in antimicrobial and antioxidative protection of food quality–A review. Trends Food Sci. Tech., 83, 5362.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Santiauo, K.B., Piana, G.M., Conti, B.J., Cardoso, E.D.O., Murbacm Teles Andrade, B. F., & Srorcin, J.M. (2018): Microbiological control and antibacterial action of a propolis-containing mouthwash and control of dental plaque in humans. Nat. Prod. Res., 32(12), 14411445.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sinuleton, V.L., Ortmorer, R. & Lamuela-Raventós, R.M. (1999): Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagent. Method. Enzymol., 299, 152178.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Velikova, M., Bankova, V., Sorkun, K., Houcine, S., Tsvetkova, I. & Kujumuiev, A. (2000): Propolis from the Mediterranean region: chemical composition and antimicrobial activity. Z. Naturforsch. C., 55(9,10), 790793.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Woods, G.L., Broyn-Elliott, B., Desmond, E.P., Hall, G.S., Heirets, L., Pryrrer, G.E. & Witebsky, F.G. (2003): Susceptibility testing of mycobacteria, nocardiae, and other aerobic actinomycetes; Approved standard. CLSI publication / Clinical and Laboratory Standards Institute, M24-A2.

    • Search Google Scholar
    • Export Citation
  • Yadav, K. & Prakasm, S. (2017): Dental caries: A microbiological approach. J. Clin. Infect Dis. Pract., 2(1), 115.

  • Amuja, A. & Amuja, V. (2010): Apitherapy–A sweet approach to dental diseases. Part I: Honey. J. Adv. Dental Res., 1, 8186.

  • Almasaudi, S.B., Al Namari, A.A., El Sayed, M., Barbour, E., Al Mumayayi, S. M., & Harakem, S. (2017): Antimicrobial effect of different types of honey on Staphylococcus aureus. Saudi J. Biol. Sci., 24(6), 12551261.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Baltas, N., Yildiz, O. & Kolayli, S. (2016): Inhibition properties of propolis extracts to some clinically important enzymes. J. Enzyme Inhib. Med. Ch., 31, 5255.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Can, Z., Yildiz, O., Şamin, H., Asadov, A. & Kolayli, S. (2015): Phenolic profile and antioxidant potential of propolis from Azerbaijan. Mellifera, 15(1), 1628.

    • Search Google Scholar
    • Export Citation
  • Kaloueropoulos, N., Konteles, S.J., Troullidou, E., Mourtzinos, I. & Karatmanos, V.T. (2009): Chemical composition, antioxidant activity and antimicrobial properties of propolis extracts from Greece and Cyprus. Food Chem., 116(2), 452461.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Keskin, M. & Kolayli, S. (2018): Standardization of propolis, is it possible? Uludag Bee J., 18(2),101110.

  • Keskin, Ş., Mayda, N., Keskin, M. & Özkök, A. (2020): Investigation of Bilecik honeys in terms of melissopalynology and chemical analyses. GIDA–J. Food, 45(2), 275289.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kolayli, S., Cakir, H.E. & Samin, H. (2016): Anti-inflammatory activities of some bee products by inhibition of bovine testes hyaluronidase. Curr. Enzyme Inhib., 12(2), 183187.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Neto, M.R., Tintino, S.R., Da Silva, A.R.P., Do Socorro Costa, M., Boliuon, A.A., & Coutinmo, H.D.M. (2017): Seasonal variation of Brazilian red propolis: Antibacterial activity, synergistic effect and phytochemical screening. Food Chem. Toxicol., 107, 572580

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Pobieua, K., Kra¿nieyska, K. & Gnieyosz, M. (2019): Application of propolis in antimicrobial and antioxidative protection of food quality–A review. Trends Food Sci. Tech., 83, 5362.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Santiauo, K.B., Piana, G.M., Conti, B.J., Cardoso, E.D.O., Murbacm Teles Andrade, B. F., & Srorcin, J.M. (2018): Microbiological control and antibacterial action of a propolis-containing mouthwash and control of dental plaque in humans. Nat. Prod. Res., 32(12), 14411445.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sinuleton, V.L., Ortmorer, R. & Lamuela-Raventós, R.M. (1999): Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagent. Method. Enzymol., 299, 152178.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Velikova, M., Bankova, V., Sorkun, K., Houcine, S., Tsvetkova, I. & Kujumuiev, A. (2000): Propolis from the Mediterranean region: chemical composition and antimicrobial activity. Z. Naturforsch. C., 55(9,10), 790793.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Woods, G.L., Broyn-Elliott, B., Desmond, E.P., Hall, G.S., Heirets, L., Pryrrer, G.E. & Witebsky, F.G. (2003): Susceptibility testing of mycobacteria, nocardiae, and other aerobic actinomycetes; Approved standard. CLSI publication / Clinical and Laboratory Standards Institute, M24-A2.

    • Search Google Scholar
    • Export Citation
  • Yadav, K. & Prakasm, S. (2017): Dental caries: A microbiological approach. J. Clin. Infect Dis. Pract., 2(1), 115.

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