EVALUATION OF THE ANTIBACTERIAL, ANTIBIOFILM, ANTIOXIDANT, AND CYTOTOXIC EFFECTS OF SOME TURKISH HONEYS

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1 EVALUATION OF THE ANTIBACTERIAL, ANTIBIOFILM, ANTIOXIDANT, AND CYTOTOXIC EFFECTS OF SOME TURKISH HONEYS OZGUR CEYLAN a*, AYSEL UGUR b, MUSTAFA ISILOGLU c, FILIZ OZCAN c a Apiculture Program, Ula Ali Kocman Vocational School, Mugla Sıtkı Koçman University, Ula- Mugla, TURKEY b Department of Basic Sciences, Section of Medical Microbiology, Faculty of Dentistry, Gazi University, Emek, Ankara, TURKEY c Department of Biology, Faculty of Sciences, Mugla Sıtkı Koçman University, Kotekli-Mugla, TURKEY XXXXIII International Apicultural Congress

2 CONTENTS The aim of the study Introduction Material and Methods Results and Discussion Conclusion

3 The aim of our study was to investigate the antibacterial, antibiofilm, antioxidant and cytotoxic activity of nine Turkish honey samples collected, from different localities of Turkey.

4 INTRODUCTION

5 Honey has been used since ancient time mainly as sweetening agent but also for therapeutic uses. It is the most natural products having a large variance in therapeutic components depending on its origin. Thus, the floral source of honey plays an important role on its biological properties (Molan, 2002).

6 Although the honey therapeutic action has been considered by researchers, studies only have been carried out on screening the raw honey samples on antimicrobial activity (Taormina et al., 2001; Al-Mamary et al., 2002; Kucuk et al., 2007; Basualdo et al., 2007; Estevinho et al., 2008; Truchado et al., 2009; Alvarez-Suarez et al., 2010; Gomes et al., 2010; Silici et al, 2010) and on antioxidant capacity (Rauha et al., 2000; Frankel et al., 1998; Estevinho et al., 2008; Alvarez-Suarez et al., 2010; Silici et al, 2010). To our knowledge, there are limited studies on the antibiofilm (Badet and Quero 2011) and cytotoxic activity (Jaganathan et al., 2010) of the honeys.

7 MATERIALS AND METHODS

8 Honey samples A total nine of honey samples, from different localities of Turkey, were directly collected through beekeepers. Table 1. Geographical origins of honey samples studied. Sample code Region of Turkey Type B-1 Nevsehir Pumpkin B-2 Zonguldak Chestnut B-3 Muğla-Datca Thyme B-4 Gaziantep Herba euphorbiae B-5 Muğla- Marmaris Chaste (Vitex agnus-castus) B-6 Van-Muradiye Multifloral B-7 Muğla-Gökova Eucalyptus B-8 Muğla-Bodrum Honeydew B-9 Muğla-Milas Honeydew

9 Bacterial Strain and Culture Conditions The bacterial strains used as test organisms were Bacillus subtilis (ATCC 6633), Staphylococcus aureus (ATCC 25923), Staphylococcus aureus (MU 40), Staphylococcus epidermidis (MU 30), Streptococcus mutans (ATCC 35668) and Listeria monocytogenes (ATCC 7644). The strains were obtained from the Mugla University Culture Collection. The above-mentioned bacteria, except S.mutans, were cultured in nutrient broth (NB) (Difco, USA), S.mutans was cultured in Brain Heart Infusion Broth (BHIB)(Difco). The strains were incubated at 37±0.1ºC for h.

10 Screening of antimicrobial activity in honey samples. Antimicrobial activity of honey samples was assessed by agar well diffusion method and also minimum inhibition concentrations (MICs) was detected by microdilution broth technique.

11 Microplate biofilm assay The antibiofilm effect of subinhibitory concentrations of honey samples were analyzed by the microplate biofilm assay (Merritt et al., 2005).

12 Antioxidant assay to determine DPPH scavenging activity Antioxidant capacity was determined in terms of their antiradical capacity using the stable free radical 1,1-diphenyl-2-picryl hydrazyl (DPPH) (Burits and Bucar, 2000; Cuendet et al., 1997).

13 Brine shrimp lethality bioassay The cytotoxic activity of the honey samples were evaluated using brine shrimp lethality bioassay method (Meyer et al., 1982). Brine shrimps (Artemia salina Leach) nauplii (Ocean 90, USA) were used to be test organisms.

14 Statistical analysis The median lethal concentration (LC 50 ) and 95% confidence intervals of the test samples were calculated using the probit analysis method described by Finney (1971), as the measure of toxicity of the honey solutions.

15 RESULTS AND DISCUSSION

16 The results of the antibacterial investigations using the agar-well diffusion method are given in Table 2. It indicates that different bacterial species demonstrated different levels of sensitivities towards the tested honey samples. The diameter for zone of inhibition for honey samples ranged from 34 to 9 mm at 75% honey concentration used. Maximum inhibitory effect was on B. subtilis and minimum inhibitory effect was on S.mutans and L.monocytogenes. Table 2. Antibacterial activity of honeys using agar-well diffusion method Inhibition zone diameter (mm) Test bacteria B. subtilis ATCC :No inhibition zone, P: Penicilline (10 IU), AM:Ampicillin (10 mcg) The results are given in the table only 75% honey concentrations. Honey samples Antibiotics B-1 B-2 B-3 B-4 B-5 B-6 B-7 B-8 B-9 P AM S. aureus ATCC S. aureus MU S. epidermidis MU S. mutans ATCC L. monocytogenes ATCC

17 Results pertaining to the antibacterial investigations using the microdilution broth technique are given in Table 3. Table 3. Minimal inhibitory concentration (MIC) values of honeys Honey samples Antibiotics Test bacteria B-1 B-2 B-3 B-4 B-5 B-6 B-7 B-8 B-9 AM OX MIC (mg/ml) B. subtilis ATCC ,156 0,156 S. aureus ATCC ,156 0,156 S. aureus MU ,625 0,156 S. epidermidis MU ,312 0,078 S. mutans ATCC ,156 0,312 L. monocytogenes ATCC ,625 0,625 -: No inhibition, AM: Ampicillin, OX: Oxytetracycline

18 MIC values obtained were mg/ml against tested bacteria. The honey samples showed highest antibacterial activity to B.subtilis and S.aureus ATCC In addition, S.aureus MU40 and S.epidermidis MU 30 were moderately sensitive to the antimicrobial activity of B-2, B-5, B-6, B-8 and B-9 honey samples. However, S.mutans and L.monocytogenes were the most resistant microorganisms. The high antibacterial activity against all bacteria tested in B-6 (Van-Muradiye, multifloral honey) were determined.

19 The inhibitory effects on tested bacteria biofilm formation of the honey solutions is shown Table 4. Honey samples Concentration B-1 B-2 B-3 B-4 B-5 B-6 B-7 B-8 B-9 Test bacteria B. subtilis ATCC 6633 S. aureus ATCC S. aureus MU 40 S. epidermidis MU 30 S. mutans ATCC L. monocytogenes ATCC 7644 mg/ml Percentage (%) inhibition 37.5 NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT 8.87 NT NT NT NT - NT NT - - NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT NT - - NT NT NT NT NT NT NT NT NT 25 NT NT NT NT NT NT NT NT 12.5 NT NT NT NT NT 9.3 NT NT NT 6.25 NT NT NT NT NT - NT NT NT 50 NT NT NT NT NT NT NT NT 37.5 NT NT NT NT NT NT NT NT 25 NT NT NT NT NT 17.8 NT NT NT 12.5 NT NT NT NT NT 6.23 NT NT NT

20 All honey samples inhibited B.subtilis biofilm formation at sub- MIC levels. Also all honey samples, except B-1, reduced S.aureus ATCC biofilm formation at various percentage. S.aureus MU 40 and S.epidermidis MU 30 biofilm formations were reduced by B-5, B-6 and B-8 honey samples. Only B-6 showed antibiofilm activity to S.mutans and L.monocytogenes. S.mutans biofilm formation was reduced up to 27.77% by MIC as 37.5 mg/ml of B6 honey sample. The B-6 in MIC concentration reduced the L.monocytogenes biofilm formation to 41.05%.

21 The results obtained for DPPH radical scavenging activity of these honeys are summarized in Table 5. Table 5. IC 50 values a (mg/ml) of honey extracts in DPPH scavenging assays Sample DPPH (IC a 50 ) B B B B B B B B B-9 71 BHT 0.48 Alpha-tocoferol 1.75 a IC 50 (mg/ml): Effective concentration at which 50% of DPPH radicals are scavenged.

22 The IC 50 values of samples using free radical scavenging assay were determined. The obtained IC50 values of samples showed a high variability depending on the source of honey. The lowest value in IC 50 values was determined in B-6 as mg/ml. As it was expected, B-8 and B-9 showed a lower values and the values was found to be 43.5 and 71 mg/ml, in accordance with recent studies that have found that the darkest coloured honeys present the highest antioxidant capacity (McKibben and Engeseth, 2002; Gheldof and Engeseth, 2002; Vela et al., 2007). According to our results, honey samples showed a good correlation between antioxidant capacity and antibacterial/antibiofilm activity.

23 The LC 50 values of the brine shrimp lethality bioassay obtained for honey extracts and that of the positive control, Vincristine sulphate, have been presented in Table 6. Table 6. Cytotoxic activity of honey samples on brine shrimp nauplii. Honey number LC50 (µg/ml) Solution(ppm) Number of dead 95% confidence The degree of organisms interval toxicity B-1 LC/EC B-2 LC/EC B-3 LC/EC B-4 LC/EC B-5 LC/EC B-6 LC/EC B-7 LC/EC B-8 LC/EC B-9 LC/EC Vincristine LC/EC Non-toxic toxic harmful Non-toxic Non-toxic harmful toxic Non-toxic toxic Highly toxic

24 Three of honey samples (B-2, B-7 and B-9) exhibited significant toxicity towards brine shrimps. The LC 50 values of these samples were within the range of ca 15.9 to 87.0 µg/ml. Whereas positive control (Vincristine sulphate) was 0.42 µg/ml. These honey samples can be considered to be a promising candidate for a food derived anticancer compound. LC 50 values obtained by the 4 honey samples (B-1, B-4, B-5, B- 8) were classified as non-toxic, the 2 samples (B-3 and B-6) were classified as harmful.

25 Brine shrimp lethality assay can be preferred in detecting of antitumour and pesticidal compounds due to its simplicity and low cost (Mazid et al., 2008). In vitro studies are of importance in view of further studies planned in in vivo conditions on antitumour activity of honey samples displaying cytotoxicity. Honey extracts with significant cytotoxic activity should also be tested on animal models in order to confirm their antitumour activities. Selecting the novel anticancer agents, this step is required to eliminate cytotoxic compounds with little value for further investigation.

26 CONCLUSION

27 All honey samples showed the highest antibacterial activity against Bacillus subtilis. A number of honey samples have promising antibacterial activity against Staphylococci which causing various infectious diseases. Especially B-6 has showed antibacterial activity to all tested microorganisms including S.mutans and L.monocytogenes. B-6 is also able to inhibit the formation of biofilms in different proportions all tested microorganisms. Antibiofilm and antibacterial activity results have shown well-correlation within each other. B-6 has the highest scavenging activity on DPPH radicals, which can be related to the antioxidant activity Whereas B-2, B-7 and B-9 displayed the maximum toxicity towards Brine shrimps. Further studies are required to study on constituents of B-2, B-7 and B-9 honey samples due to their prominent antitumour activity.

28 Thank you for your attention

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