Antimicrobial activities of natural honeys and royal jellys on some pathogenic bacteria

Year 2022, Volume: 24 Issue: 2, 672 - 689, 08.07.2022

Seda Oğur , Yusuf Dayan

Abstract

In this study aimed to determine antimicrobial activities of natural honeys (HN) in Bitlis, and natural royal jellys (RJ) in Bitlis & Ağrı on some pathogenic bacteria (Escherichia coli (ATCC 25922), Pseudomonas aeruginosa (ATCC 27853), Staphylococcus aureus (ATCC 29213), Enterococcus faecalis (ATCC 29212), Listeria monocytogenes (ATCC 7644), Streptococcus pyogenes (ATCC 19615), Salmonella Enteritidis (ATCC 13076) and Bacillus cereus (ATCC 11778)). HN and RJ samples at concentrations of 10%, 25%, 50% and 100% were used to identify their antimicrobial activities using the method of hollow agar. 50 μL of each HN and RJ concentrates was inoculated into the wells. The diameters of inhibition zone occurring in petri dishes were measured in millimeters (mm) at the end of the incubation at 37 °C for 24 hours. It was observed that the largest diameters of inhibition zones were in 100% concentrates; whereas, no zones occurred in 10% concentrate. The sample with the most antimicrobial activity was the honey sample (HN1) obtained from the Bitlis Dere region, with an inhibition zone of 39.50±4.93 mm on P. aeruginosa (ATCC 27853). 100% and 50% concentrates of RJ samples had antimicrobial activities on all bacteria strains except S. pyogenes (ATCC 19615). The results of the present study provided preliminary evidence that the examined bee products have potential for use in apitherapy applications.

Keywords

Honey, Royal Jelly, Antimicrobial activity, Pathogenic bacteria, Inhibition zone

Supporting Institution

Tubitak BIDEB

Project Number

1919B01160321

Thanks

We would like to thank Tubitak BIDEB for supporting this study with the project number 1919B01160321.

Doğal balların ve arı sütlerinin bazı patojenik bakteriler üzerindeki antimikrobiyal aktivitesi

Abstract

Bu çalışmada Bitlis’teki doğal balların (BL) ve Bitlis ve Ağrı’daki doğal arı sütlerinin (AS) bazı patojenik bakteriler (Escherichia coli (ATCC 25922), Pseudomonas aeruginosa (ATCC 27853), Staphylococcus aureus (ATCC 29213), Enterococcus faecalis (ATCC 29212), Listeria monocytogenes (ATCC 7644), Streptococcus pyogenes (ATCC 19615), Salmonella Enteritidis (ATCC 13076) and Bacillus cereus (ATCC 11778)) üzerindeki antimikrobiyal aktivitesini belirlemek amaçlanmıştır. Oyuk agar metodu kullanılarak antimikrobiyal aktivitelerini tanımlamak için BL ve AS numuneleri %10’luk, %25’lik, %50’lik ve %100’lük konsantrasyonlarda kullanılmıştır. BL ve AS konsantratlarından her bir kuyucuğa 50 μL inoküle edilmiştir. 37 °C’de 24 saatlik inkübasyondan sonra petrilerde oluşan inhibisyon zonları milimetre (mm) olarak ölçülmüştür. En büyük inhibisyon zonu çapları %100’lük konsantratlarda gözlemlenirken, %10’luk konsantratlarda zon oluşmamıştır. En iyi antimikrobiyal aktiviteye sahip numune P. aeruginosa (ATCC 27853) üzerinde 39,50±4,93 mm inhibisyon zonu oluşturan, Bitlis Dere mevkiinden elde edilen BL1 numunesi olmuştur. AS numunelerinin %100’lük ve %50’lik konsantratları S. pyogenes (ATCC 19615) dışındaki tüm bakteri suşları üzerinde antimikrobiyal aktiviteye sahip olmuştur. Bu çalışmanın sonuçları, incelenen arı ürünlerinin apiterapi uygulamalarında kullanım potansiyeline sahip olduğuna dair ön kanıtlar sağlamıştır.

Keywords

Bal, Arı sütü, Antimikrobiyal aktivite, Patojenik bakteri, İnhibisyon zonu

Project Number

1919B01160321

References

• Republic of Turkey Ministry of Health, The Regulation on Traditional and Complementary Medicine Practices, (2014). http://www.mevzuat.gov.tr/MevzuatMetin/yonetmelik/7.5.20164-ek.pdf, (18.01.2022)
• Ozturk, O. and Selcuk, M. Y., Apitherapy in primary care, Turkish Journal of Family Medicine and Primary Care, 10, 3, 124–125, (2016).
• Hisil, Y. and Borekcioglu, N., The composition of honey and honey tricks, Gıda (The Journal of Food), 2, 79–82, (1986).
• Mundo, M. A., Padilla-Zakour, O. I. and Worobo, R. W., Growth inhibition of foodborne pathogens and food spoilage organisms by select raw honeys, International Journal of Food Microbiology, 97, 1, 1–8, (2004).
• Molan, P. C., The evidence supporting the use of honey as a wound dressing, International Journal of Lower Extremity Wounds, 5, 1, 40–54, (2006).
• Simon, A., Traynor, K., Santos, K., Blaser, G., Bode, U. and Molan, P. C., Medical Honey for Wound Care-Still the 'Latest Resort'?, Evidence-based Complementary and Alternative Medicine, 6, 2, 165–173, (2008).
• Molan, P. C., Honey as an antimicrobial agent, Proceedings, International Conference on Bee Product: Properties, Applications and Apitherapy Israel, p: 27, (1997).
• Jeffrey, A. E. and Echazarreta, C. M., Medicinal uses of honey, Revista Biomedica, 7, 1, 43–49, (1996).
• Aslan, A. and Bayraktar, A., Chemical composition and importance of royal jellys, Proceedings, Congress of Food Engineering Gaziantep, Turkey, p. 339–349, (1996).
• Ozturk, O., Health effects of bee products, (2012). http://www.balder.org.tr/sunumlar/AUSUE_Semineri_Prof_Dr_Oguz_Ozturk_sunumu_(No_13).pdf, (05.01.2022).
• Fontana, R., Mendes, M. A., de Souza, B. M., Konno, K., César, L. M., Malaspina, O. and Palma, M. S., Jelleines: A family of antimicrobial peptides from the Royal jelly of honeybees (Apis mellifera), Peptides, 25, 6, 919–928, (2004).
• Cagliyan, A., Beekeeping activities in Bitlis, Journal of Geography, 30, 1–25, (2015).
• Kaya, F., Structure of beekeeping in Ağrı and evaluation status, The Journal of Social Sciences Institute of Ataturk University, 12, 2, 35–55, (2008).
• Alan, Y., Atalan, E., Erbil, N., Bakir, O., Orman, Z. and Panik, P., Investigation of antimicrobial activity of honey and propolis collected in Mus and Bitlis region, Mus Alparslan University Journal of Science, 2, 1, 221–229, (2014).
• Collins, C. H. and Lyne P. M., Microbiological methods, Butterworth and Co. (Publishers) Ltd., London, UK, (1985).
• Anonymous, NCCLS (National Committee for Clinical Laboratory Standards). Performance standards for antimicrobial susceptibility testing, The 9th International Supplement; M100-S9, Villanova, PA, United States Commonwealth of Pennsylvania, (1999).
• Valgas, C., Souza, S. M. D., Smânia, E. F. and Smânia, Jr. A., Screening methods to determine antibacterial activity of natural products, Brazilian Journal of Microbiology, 38, 2, 369–380. (2007). doi.org/10.1590/S1517-83822007000200034
• Anonymous, IBM SPSS Statistics for Windows, Version 25.0. New York, USA: IBM Corp, Armonk, (2017).
• Aksoy, Z. and Digrak, M., In vitro studies on antimicrobial effects of honey and propolis gathered in Bingol region, Fırat University Turkish Journal of Science and Technology, 18, 4, 471–478, (2006).
• Olaitan, P. B., Adeleke, O. E. and Ola, I. O., Honey: a reservoir for microorganisms and an inhibitory agent for microbes, African Health Sciences, 7, 3, 159–165, (2007).
• Scmidtchen, A., Holst, E., Topper, H., Bjorck, L., Elastase–producing Pseudomonas aeruginosa degrade plasma proteins and extracellular products of human skin and fibroblasts, and inhibit fibroblast growth, Microbial Pathogenesis, 34, 1, 47–55, (2003).
• Bilgehan, H., Clinical microbiology (special bacteriology), Baris Publications, Izmir, Turkey, (2000).
• Mengeloglu, F. Z., Terzi, H. A. and Bilici, M., A case report with catheter caused Bacillus cereus bacteremia and investigating the clonal relatedness between the isolates by PFGE, Dicle Medical Journal, 38, 3, 358–360, (2011).
• Ryan, K. J. and Ray, C. G., (2004) Sherris medical microbiology (4th ed.), Mc Graw Hill, New York, USA, (2004).
• Goulet, V., Jacquet, C., Martin, P., Vaillant, V., Laurent, E. and de Valk, H., Surveillance of human listeriosis in France, 2001-2003, Euro Surveillanca, 11, 6, 79–81, (2006).
• Kara, A., Parlakay, A. O., Gur, D., Cengiz, A. B., Tezer, H., Ciftci, E., Keser, M., Ozen, M., Kantaroglu, O. C., Tutanc, M., Salihoglu, B., Yuksekkaya, S., Celikel, E., Ince, E., Arica, V., Hatipoglu, S., Odabas, D., Altay, F., Karbuz, A. and Ceylan, M., Turkey resistance evaluation pilot study results of group a beta hemolytic Streptococcus, Journal of Pediatric Infection, 5, 3, 96–99, (2011).
• Erdem, B., Salmonella serotyped in 1998-2000, Turkish Journal of Infection, 15, 137–140, (2001).
• Acheson, D. and Hohmann, E. L., Nontyphoidal salmonellosis, Clinical Infectious Diseases, 32, 2, 263–269, (2001).
• Ogbu, K. I., Ochai, S. O., Olabode, M. P., Olaolu, O.S. and Maimadu, A. A., Comparative study on the antibacterial activities of bee product (propolis, pollen, bee wax and honey), IOSR Journal of Pharmacy and Biological Sciences (IOSR-JPBS), 13, 2-II, 20–27, (2018). doi: 10.9790/3008-1302022027
• Erdogrul, O. and Erbilir, F., Investigation of microbial quality and antimicrobial effects of honey samples produced in Kahramanmaras, Kahramanmaras Sutcu Imam University Journal of Engineering Sciences, 10, 1, 1–5, (2007).
• Polat, I., Investigation of antimicrobial, antioxidant activities, pesticide and antibiotic residues of some honey produced in the south Marmara region, MSc Thesis, Balikesir University, Instiyute of Science, Balıkesir, Turkey, (2011).
• Cooper, R., The use of honey as an antiseptic in managing Pseudomonas infections, Journal of Wound Care, 8, 4, 161–164, (1999).
• Cooper, R. A., Halas, E. and Molan, P. C., The efficacy of honey in inhibiting strains of Pseudomonas aeruginosa from infected burns, Journal of Burn Care & Rehabilation, 23, 6, 366–370, (2002).
• Obaseiki-Ebor, E. E., Afonya, T. C. A. and Onyekweli, A. O., Preliminary report on the antimicrobial activity of honey distillate, Journal of Pharmacy and Pharmacology, 35, 11, 748–749, (1983).
• Obaseiki-Ebor, E. E. and Afonya, T. C. A., In vitro evaluation of the anticandidiasis activity of honey distillate (HY-1) compared with that of some antimycotic agents, Journal of Pharmacy and Pharmacology, 36, 4, 283–284, (1984).
• Malika, N., Mohamed, F. and Chakib, E. A., Antimicrobial activities of natural honey from aromatic and medicinal plants on antibio-resistant strains of bacteria, International Journal of Agriculture & Biology, 6, 2, 289–293, (2004).
• Dastouri, M. R., Fakhimzadeh, K., Shayeg, J., Dolgari-Sharaf, J., Valilou, M. R., Maheri-Sis, N., Evaluating antibacterial activity of the Iranian honey through MIC method on some dermal and intestinal pathogenic bacteria, Journal of Animal and Veterinary Advances, 7, 4, 409–412, (2008).
• Omafuvbe, B. O. and Akanbi, O. O., Microbiological and physico-chemical properties of some commercial Nigerian honey, African Journal of Microbiology Research, 3, 12, 891–896, (2009).
• Dogan, H., Determination of chemical, physical and antimicrobial properties of flower honeys, MSc Thesis, Ataturk University, Institute of Science, Erzurum, Turkey, (2014).
• Karadal, F., Ertas Onmaz, N., Abay, S., Yildirim, Y., Al, S., Tatyuz, I. and Akcay, A., A study of antibacterial and antioxidant activities of bee products: propolis, pollen and honey samples, The Ethiopian Journal of Health Development, 32, 2, 116–122, (2018).
• Khalil, A. T., Khan, I., Ahmad, K., Khan, Y. A., Khan, M. and Khan, M. J., Synergistic antibacterial effect of honey and Herba Ocimi Bacilici against some bacterial pathogens, Journal of Traditional Chinese Medicine, 33, 6, 810–814, (2013).
• Pesavento, G., Ducci, B., Comodo, N. and Lo Nostro, A., Antimicrobial resistance profile of Staphylococcus aureus isolated from raw meat: A research for methicillin resistant Staphylococcus aureus (MRSA), Food Control, 18, 3, 196–200, (2007).
• Oncul, O., Erdemoglu, A., Ozsoy, M. F., Altunay, H., Ertem, Z. and Cavusoglu, S., Nasal Staphylococcus aureus carriage in healthcare staff, Klimik Journal, 15, 3, 74–77, (2002).
• Garcia-Amoedo, L. H. and de Almeida-Muradian, L. B., Determination of trans-10-hydroxy-2-decanoic acid (10-HDA) in royal jelly from São Paulo State, Brazil, Food Science and Technology (Campinas), 23, 62–65, (2003).
• Eshraghi, S. and Seifollahi, F., Antibacterial effects of royal jelly on different strains of bacteria, Iranian Journal of Public Health, 32, 1, 25–30, (2003).
• Ramanathan, A. N. K. G., Krishna, A., Nair, A. J. and Sugunan, V. S., Antimicrobial activity of royal jelly from Indian honeybee, Apis cerana, International Journal of Allied Practice, Research and Review, V, II, 07–12, (2018).
• Garcia, M. C., Finola, M. S. and Marioli, J. M., Antibacterial activity of Royal Jelly against bacteria capable of infecting cutaneous wounds, Journal of ApiProduct and ApiMedical Science, 2, 3, 93–99, (2010). doi: 10.3896/IBRA.4.02.3.02
• Ratanavalachai, T. and Wongchai, V., Antibacterial activity of intact Royal Jelly, its lipid extract and its defatted extract, Thammasat International Journal of Science and Technology, 7, 1, 5–12, (2002).
• Garcia, M. C., Finola, M. S. and Marioli, J. M., Bioassay directed identification of Royal Jelly’s active compounds against the growth of bacteria capable of infecting cutaneous wounds, Advances in Microbiology, 3, 138–144, (2013). http://dx.doi.org/10.4236/aim.2013.32022
• Boukraa, L., Meslem, A., Benhanifia, M., Hammoudi, S. M., Synergistic effect of starch and Royal Jelly against Staphylococcus aureus and Escherichia coli, The Journal Alternative and Complementary Medicine, 15, 755–757, (2009). http://dx.doi.org/10.1089/acm.2008.0483
• Moselhy, W. A., Fawzy. A. M. and Kamel, A. A., An evaluation of the potent antimicrobial effects and unsaponifiable matter analysis of the Royal Jelly, Life Science Journal, 2, 10, 290–296, (2013).
• Boukraa, L., Additive activity of Royal Jelly and honey against Pseudomonas aeruginosa, Alternative Medicine Review, 13, 4, 330–333, (2008).
• Bilikova, K., Huang, S. C., Lin, I. P., Simuth, J. and Peng, C. C., Structure and antimicrobial activity relationship of royalisin, an antimicrobial peptide from Royal Jelly of Apis mellifera, Peptides, 68, 190–196, (2015). http://dx.doi.org/10.1016/j.peptides.2015.03.001
• Eshraghi, S., An evaluation of the potent inhibitory effects of Royal Jelly fractions against Streptomyces bacteria, Pakistan Journal of Medical Sciences, 21, 1, 63–68, (2005).
• Melliou, E. and Chinou, I., Chemistry and bioactivity of royal jelly from Greece, Journal of Agricultural and Food Chemistry, 53, 23, 8987–8992, (2005). doi: 10.1021/jf051550p
• Alreshoodi, F. M. and Sultanbawa, Y., Antimicrobial activity of royal jelly, Anti-Infective Agents, 13, 1, 50–59, (2015). doi: 10.2174/2211352513666150318234430
• Fujiwara, S., Imai, J., Fujiwara, M., Yaeshima, T., Kawashima, T. and Kobayashi, K., A potent antibacterial protein in royal jelly Purification and determination of the primary structure of royalisin, The Journal of Biological Chemistry, 265, 19, 11333–11337, (1990).
• Biliková, K., Hanes, J., Nordhoff, E., Saenger, W., Klaudiny, J. and Šimúth, J., Apisimin, a new serine–valine-rich peptide from honeybee (Apis mellifera L.) royal jelly: purification and molecular characterization, FEBS Letters, 528, 1–3, 125–129, (2002).
• Romanelli, A., Moggio, L., Montella, R. C., Campiglia, P., Iannaccone, M., Capuano, F., Pedone, C. and Capparelli, R., Peptides from Royal Jelly: studies on the antimicrobial activity of jelleins, jelleins analogs and synergy with temporins. Journal of Peptide Science, 17, 5, 348–352, (2011). http://dx.doi.org/10.1002/psc.1316