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INHIBITORY EFFECTS of HONEY on STAPHYLOCOCCUS AUREUS and ESCHERICHIA COLI: A CURRENT REVIEW

Year 2023, Volume: 14 Issue: 3, 133 - 148, 30.12.2023
https://doi.org/10.38137/vftd.1385968

Abstract

Honey is a natural food that has been used since ancient times for its medicinal benefits. Thanks to its antimicrobial activity, which has a very important place among honey's medicinal effects, it can be used against various pathogens such as Staphylococcus aureus and Escherichia coli. The antibacterial effect of honey depends on physical (high osmotic pressure, low water activity and low pH value), chemical (hydrogen peroxide, methylglyocal, phenolic compounds, flavonoids, organic acids and proteins) and biological factors (enzymes secreted by bees, probiotic bacteria and pollen). The antibacterial effect of honey can be affected by the origin of the honey, the type of flower obtained, the season of harvest and processing methods. Therefore, more studies are required to clearly demonstrate the antimicrobial activity of honey and make it available for use in clinical treatments. In this review, it was aimed to better understand the antimicrobial effects of honey on S. aureus and E. coli by searching the current literature.

References

  • Adeyemo, R. O., Torimiro, N., Akinola, S. A., Lawal, S. K., Abolarinwa, T. O. & Adewoye, W. O. (2017). Study on antibacterial effi cacy of diff erent honey types in South Western Nigeria against wound associated bacteria. Journal of Apitherapy, 2, 15-19.
  • Afroz, R., Tanvir, E. M., Zheng, W. & Little, P. J. (2016). Molecular Pharmacology of Honey. Clinical and Experimental Pharmacology, 06.
  • Akyalçın, H. & Süerdem, T. B. (2017). In Vitro Screening of Antibacterial Activity of Honey Samples Collected from Kosovo. Journal of Scientific Perspectives, 1, 31–40.
  • Almasaudi, S. B., Al-Nahari, A. A. M., Abd El-Ghany, E. S. M., Barbour, E., Al Muhayawi, S. M., Al-Jaouni, S., Azhar, E., Qari, M., Qari, Y. A. & Harakeh, S. (2017). Antimicrobial effect of different types of honey on Staphylococcus aureus. Saudi Journal of Biological Sciences, 24, 1255–1261.
  • Asma, S. T., Bobiş, O., Bonta, V., Acaroz, U., Shah, S. R. A., Istanbullugil, F. R. & Arslan-Acaroz, D. (2022a). General Nutritional Profile of Bee Products and Their Potential Antiviral Properties against Mammalian Viruses. Nutrients, 14, 3579.
  • Asma, S. T., Imre, K., Morar, A., Imre, M., Acaroz, U., Shah, S. R. A., Hussain, S. Z., Arslan-Acaroz, D., Istanbullugil, F. R., Madani, K., Athanassiou, C., Atanasoff, A., Morar, D., Herman, V. & Zhu, K. (2022b). Natural Strategies as Potential Weapons against Bacterial Biofilms. Life, 12.
  • Bazaid, A. S., Alsolami, A., Patel, M., Khateb, A. M., Aldarhami, A., Snoussi, M., Almusheet, S. M. & Qanash, H. (2023). Antibiofilm, Antimicrobial, Anti-Quorum Sensing, and Antioxidant Activities of Saudi Sidr Honey: In Vitro and Molecular Docking Studies. Pharmaceutics, 15, 2177.
  • Ciupescu, L. M., Auvray, F., Nicorescu, I. M., Meheut, T., Ciupescu, V., Lardeux, A. L., Tanasuica, R. & Hennekinne, J. A. (2018). Characterization of Staphylococcus aureus strains and evidence for the involvement of non-classical enterotoxin genes in food poisoning outbreaks. FEMS Microbiology Letters, 365.
  • Çakır, Y., Çobanoğlu, D. N., Dervişoğlu, G., Koçyiğit, S., Karahan, D. & Yelkovan, S. (2020). Determination of Antimicrobial Activity, Palynological Characteristics and Chemical Composition of Some Honey Samples from Turkey. Mellifera, 20, 41-60.
  • Çakır, Y. & Dervişoğlu, G. (2022). Antimicrobial Effect of Honeys Collected in Bingol Region. MAS Journal of Applied Sciences, 7, 537–544.
  • Çakmak, Ö., Acaröz, U. & Gün, H. (2022). Halk Sağlığı Açısından Önemli Gıda Kaynaklı Viral Etkenler. Veteriner Farmakoloji ve Toksikoloji Derneği Bülteni, 13, 11–25.
  • David, M. Z. & Daum, R. S. (2017). Treatment of Staphylococcus aureus Infections. Current Topics in Microbiology and Immunology, 409, 325-383.
  • Fratianni, F., De Giulio, B., d’Acierno, A., Amato, G., De Feo, V., Coppola, R. & Nazzaro, F. (2023). In Vitro Prebiotic Effects and Antibacterial Activity of Five Leguminous Honeys. Foods, 12, 3338.
  • Gambo, S. B, Ali, M., Diso, S. U. & Abubakar, N. S. (2018). Antibacterial Activity of Honey Against Staphylococcus aureus and Pseudomonas aeruginosa Isolated from Infected Wound. Archives of Pharmacy & Pharmacology Research, 1, 1-6.
  • Gkoutzouvelidou, M., Panos, G., Xanthou, M. N., Papachristoforou, A. & Giaouris, E. (2021). Comparing the Antimicrobial Actions of Greek Honeys from the Island of Lemnos and Manuka Honey from New Zealand against Clinically Important Bacteria. Foods, 10, 1402.
  • Kalidasan, G., Saranraj, P., Ragul, V. & Sivasakthi, S. (2017). Antibacterial Activity of Natural and Commercial Honey-A Comparative Study. Advances in Biological Research, 11, 365-372.
  • Kara, R., Acaröz, U., Gürler, Z., Soylu, A. & Küçükkurt, O. (2019). Taze Marul Örneklerinde Esherichia coli O157 ve Listeria monocytogenes Varlığının Belirlenmesi. Avrupa Bilim ve Teknoloji Dergisi, 16, 870–873.
  • Karaynir, A. (2021). Çevresel Örneklerden Escherichia coli DH10B Suşuna Karşı Litik Bakteriyofaj İzolasyonu ve Klinik Escherichia coli Suşlarına Karşı Etkinliklerinin Belirlenmesi. Aydın, Turkey, Thesis of MSc, AMU, diss.
  • Küçükbüğrü, N. & Acaröz, U. (2020). Gıdalarda Antibiyotik Kalıntıları ve Halk Sağlığına Etkileri. Veteriner Farmakoloji ve Toksikoloji Derneği Bülteni, 11, 161–167.
  • Kumari, I., Hajam, Y. A., Thiyagarajan, K., Giri, A. & Kumar, R. (2023). Evaluation of antioxidant and antibacterial potential of honey produced from stimulative diet fed bee colonies. Discover Sustainability, 4.
  • Mahmood, A. L., Lani, M. N., Hassan, Z., Razak, S. B. A. & Ahmad, F. T. (2021). Antioxidant and antimicrobial properties of Indo-Malayan stingless bee (Heterotrigona itama) honey from different seasons and distribution of flowers. Food Research, 5, 498–507.
  • McArdle, C., Coyle, S. & Santos, D. (2023). The impact of wound pH on the antibacterial properties of Medical Grade Honey when applied to bacterial isolates present in common foot and ankle wounds. An in vitro study. Journal of Foot and Ankle Research, 16.
  • Mundo, M. A., Padilla-Zakour, O. I. & Worobo, R. W. (2004). Growth inhibition of foodborne pathogens and food spoilage organisms by select raw honeys. International Journal of Food Microbiology, 97, 1–8.
  • Oğur, S. & Dayan, Y. (2022). Antimicrobial activities of natural honeys and royal jellys on some pathogenic bacteria. BAUN Fen Bilimleri Enstitüsü Dergisi, 24, 672–689.
  • Postali, E., Peroukidou, P., Giaouris, E. & Papachristoforou, A. (2022). Investigating Possible Synergism in the Antioxidant and Antibacterial Actions of Honey and Propolis from the Greek Island of Samothrace through Their Combined Application. Foods, 11, 2041.
  • Ro Me Busserolles, J., Gueux, E., Rock, E., Mazur, A. & Rayssiguier, Y. (2002). Substituting Honey for Refined Carbohydrates Protects Rats from Hypertriglyceridemic and Prooxidative Effects of Fructose. The Journal of Nutrition. 132, 3379-3382.
  • Russo, N., Di Rosa, A. R., Pino, A., Mazzeo, G., Liotta, L., Caggia, C. & Randazzo, C. L. (2023). Assessment of sensory properties and in vitro antimicrobial activity of monofloral Sicilian honey. Food Bioscience, 52, 102449.
  • Segueni, N., Boutaghane, N., Asma, S. T., Tas, N., Acaroz, U., Arslan-Acaroz, D., Shah, S. R. A., Abdellatieff, H. A., Akkal, S., Peñalver, R. & Nieto, G. (2023). Review on Propolis Applications in Food Preservation and Active Packaging. Plants, 12.
  • Shah, T., Ali, N., Shah, Z. & Hayat, A. (2017). Antibacterial Activity of Pakistani Honey. Pakistan Journal of Scientific and Industrial Research Series B: Biological Sciences, 2, 97-100.
  • Shalsh, F. J., Khalaf, A. M., Hafiz, M. & Al-Sultan, I. I. A. (2021). Antibacterial Properties of Local Malaysian Trigona Sp. Honey Towards Different of Pathogenic Bacteria in vitro. Diyala Agricultural Sciences Journal, 13, 1-9.
  • Shamala, T. R., Shri Jyothi, Y. & Saibaba, P. (2000). Stimulatory effect of honey on multiplication of lactic acid bacteria under in vitro and in vivo conditions. Letters in Applied Microbiology, 30, 453–455.
  • Skadins, I., Labsvards, K. D., Grava, A., Amirian, J., Tomsone, L. E., Ruško, J., Viksna, A., Bandere, D. & Brangule, A. (2023). Antimicrobial and Antibiofilm Properties of Latvian Honey against Causative Agents of Wound Infections. Antibiotics, 12, 816.
  • Suerdem, T. B. & Akyalçın, H. (2018). Screening of antimicrobial and antioxidant activity of different types of honey samples obtained from Geyikli (Çanakkale) province. Communications Faculty of Science University of Ankara Series C Biology Geological Engineering and Geophysical Engineering, 27, 69–78.
  • Wadi, M. A. (2022). In Vitro Antibacterial Activity of Different Honey Samples against Clinical Isolates. BioMed Research International, 2022, 1-8.
  • Yılmaz, E. Ş. & Aslantaş, Ö. (2017). Antimicrobial resistance and underlying mechanisms in Staphylococcus aureus isolates. Asian Pacific Journal of Tropical Medicine, 10, 1059–1064.
  • Zapata-Vahos, I. C., Henao-Rojas, J. C., Yepes-Betancur, D. P., Marín-Henao, D., Giraldo Sánchez, C. E., Calvo-Cardona, S. J., David, D. & Quijano-Abril, M. (2023). Physicochemical Parameters, Antioxidant Capacity, and Antimicrobial Activity of Honeys from Tropical Forests of Colombia: Apis mellifera and Melipona eburnea. Foods, 12, 1001.
  • Zeaki, N., Johler, S., Skandamis, P. N. & Schelin, J. (2019). The Role of Regulatory Mechanisms and Environmental Parameters in Staphylococcal Food Poisoning and Resulting Challenges to Risk Assessment. Frontiers in Microbiology, 10, 1307.
  • Zhao, Y., Zhu, A., Tang, J., Tang, C. & Chen, J. (2017). Identification and measurement of staphylococcal enterotoxin M from Staphylococcus aureus isolate associated with staphylococcal food poisoning. Letters in Applied Microbiology, 65, 27–34.

BALIN STAPHYLOCOCCUS AUREUS ve ESCHERİCHİA COLİ ÜZERİNE İNHİBİTÖR ETKİSİ: GÜNCEL DERLEME

Year 2023, Volume: 14 Issue: 3, 133 - 148, 30.12.2023
https://doi.org/10.38137/vftd.1385968

Abstract

Bal, tıbbi faydalarından dolayı eski dönemlerden beri kullanılan doğal bir gıdadır. Bal tıbbi etkileri arasında oldukça önemli yer tutan antimikrobiyal aktivitesi sayesinde, Staphylococcus aureus ve Escherichia coli gibi çeşitli patojenlere karşı kullanılabilmektedir. Balın antibakteriyel etkisi, fiziksel (yüksek osmotik basınç, düşük su aktivitesi ve düşük pH değeri), kimyasal (hidrojen peroksit, metilgliokal, fenolik bileşikler, flavonoidler, organik asitler ve proteinler) ve biyolojik faktörleri (arılar tarafından salgılanan enzimler, probiyotik bakteriler ve polen) sayesinde gerçekleşmektedir. Balın antibakteriyel etkisini balın kökeni, elde edilen çiçeğin türü, hasat yapılan mevsim ve işleme yöntemleri etkileyebilmektedir. Bundan dolayı, balın antimikrobiyal aktivitesini net bir şekilde ortaya koymak ve klinik tedavilerin kullanımına sunmak için daha fazla çalışma gerekmektedir. Bu derlemede, güncel literatür taraması yapılarak, balın S. aureus ve E. coli üzerine antimikrobiyal etkilerinin daha iyi anlaşılması hedeflendi.

References

  • Adeyemo, R. O., Torimiro, N., Akinola, S. A., Lawal, S. K., Abolarinwa, T. O. & Adewoye, W. O. (2017). Study on antibacterial effi cacy of diff erent honey types in South Western Nigeria against wound associated bacteria. Journal of Apitherapy, 2, 15-19.
  • Afroz, R., Tanvir, E. M., Zheng, W. & Little, P. J. (2016). Molecular Pharmacology of Honey. Clinical and Experimental Pharmacology, 06.
  • Akyalçın, H. & Süerdem, T. B. (2017). In Vitro Screening of Antibacterial Activity of Honey Samples Collected from Kosovo. Journal of Scientific Perspectives, 1, 31–40.
  • Almasaudi, S. B., Al-Nahari, A. A. M., Abd El-Ghany, E. S. M., Barbour, E., Al Muhayawi, S. M., Al-Jaouni, S., Azhar, E., Qari, M., Qari, Y. A. & Harakeh, S. (2017). Antimicrobial effect of different types of honey on Staphylococcus aureus. Saudi Journal of Biological Sciences, 24, 1255–1261.
  • Asma, S. T., Bobiş, O., Bonta, V., Acaroz, U., Shah, S. R. A., Istanbullugil, F. R. & Arslan-Acaroz, D. (2022a). General Nutritional Profile of Bee Products and Their Potential Antiviral Properties against Mammalian Viruses. Nutrients, 14, 3579.
  • Asma, S. T., Imre, K., Morar, A., Imre, M., Acaroz, U., Shah, S. R. A., Hussain, S. Z., Arslan-Acaroz, D., Istanbullugil, F. R., Madani, K., Athanassiou, C., Atanasoff, A., Morar, D., Herman, V. & Zhu, K. (2022b). Natural Strategies as Potential Weapons against Bacterial Biofilms. Life, 12.
  • Bazaid, A. S., Alsolami, A., Patel, M., Khateb, A. M., Aldarhami, A., Snoussi, M., Almusheet, S. M. & Qanash, H. (2023). Antibiofilm, Antimicrobial, Anti-Quorum Sensing, and Antioxidant Activities of Saudi Sidr Honey: In Vitro and Molecular Docking Studies. Pharmaceutics, 15, 2177.
  • Ciupescu, L. M., Auvray, F., Nicorescu, I. M., Meheut, T., Ciupescu, V., Lardeux, A. L., Tanasuica, R. & Hennekinne, J. A. (2018). Characterization of Staphylococcus aureus strains and evidence for the involvement of non-classical enterotoxin genes in food poisoning outbreaks. FEMS Microbiology Letters, 365.
  • Çakır, Y., Çobanoğlu, D. N., Dervişoğlu, G., Koçyiğit, S., Karahan, D. & Yelkovan, S. (2020). Determination of Antimicrobial Activity, Palynological Characteristics and Chemical Composition of Some Honey Samples from Turkey. Mellifera, 20, 41-60.
  • Çakır, Y. & Dervişoğlu, G. (2022). Antimicrobial Effect of Honeys Collected in Bingol Region. MAS Journal of Applied Sciences, 7, 537–544.
  • Çakmak, Ö., Acaröz, U. & Gün, H. (2022). Halk Sağlığı Açısından Önemli Gıda Kaynaklı Viral Etkenler. Veteriner Farmakoloji ve Toksikoloji Derneği Bülteni, 13, 11–25.
  • David, M. Z. & Daum, R. S. (2017). Treatment of Staphylococcus aureus Infections. Current Topics in Microbiology and Immunology, 409, 325-383.
  • Fratianni, F., De Giulio, B., d’Acierno, A., Amato, G., De Feo, V., Coppola, R. & Nazzaro, F. (2023). In Vitro Prebiotic Effects and Antibacterial Activity of Five Leguminous Honeys. Foods, 12, 3338.
  • Gambo, S. B, Ali, M., Diso, S. U. & Abubakar, N. S. (2018). Antibacterial Activity of Honey Against Staphylococcus aureus and Pseudomonas aeruginosa Isolated from Infected Wound. Archives of Pharmacy & Pharmacology Research, 1, 1-6.
  • Gkoutzouvelidou, M., Panos, G., Xanthou, M. N., Papachristoforou, A. & Giaouris, E. (2021). Comparing the Antimicrobial Actions of Greek Honeys from the Island of Lemnos and Manuka Honey from New Zealand against Clinically Important Bacteria. Foods, 10, 1402.
  • Kalidasan, G., Saranraj, P., Ragul, V. & Sivasakthi, S. (2017). Antibacterial Activity of Natural and Commercial Honey-A Comparative Study. Advances in Biological Research, 11, 365-372.
  • Kara, R., Acaröz, U., Gürler, Z., Soylu, A. & Küçükkurt, O. (2019). Taze Marul Örneklerinde Esherichia coli O157 ve Listeria monocytogenes Varlığının Belirlenmesi. Avrupa Bilim ve Teknoloji Dergisi, 16, 870–873.
  • Karaynir, A. (2021). Çevresel Örneklerden Escherichia coli DH10B Suşuna Karşı Litik Bakteriyofaj İzolasyonu ve Klinik Escherichia coli Suşlarına Karşı Etkinliklerinin Belirlenmesi. Aydın, Turkey, Thesis of MSc, AMU, diss.
  • Küçükbüğrü, N. & Acaröz, U. (2020). Gıdalarda Antibiyotik Kalıntıları ve Halk Sağlığına Etkileri. Veteriner Farmakoloji ve Toksikoloji Derneği Bülteni, 11, 161–167.
  • Kumari, I., Hajam, Y. A., Thiyagarajan, K., Giri, A. & Kumar, R. (2023). Evaluation of antioxidant and antibacterial potential of honey produced from stimulative diet fed bee colonies. Discover Sustainability, 4.
  • Mahmood, A. L., Lani, M. N., Hassan, Z., Razak, S. B. A. & Ahmad, F. T. (2021). Antioxidant and antimicrobial properties of Indo-Malayan stingless bee (Heterotrigona itama) honey from different seasons and distribution of flowers. Food Research, 5, 498–507.
  • McArdle, C., Coyle, S. & Santos, D. (2023). The impact of wound pH on the antibacterial properties of Medical Grade Honey when applied to bacterial isolates present in common foot and ankle wounds. An in vitro study. Journal of Foot and Ankle Research, 16.
  • Mundo, M. A., Padilla-Zakour, O. I. & Worobo, R. W. (2004). Growth inhibition of foodborne pathogens and food spoilage organisms by select raw honeys. International Journal of Food Microbiology, 97, 1–8.
  • Oğur, S. & Dayan, Y. (2022). Antimicrobial activities of natural honeys and royal jellys on some pathogenic bacteria. BAUN Fen Bilimleri Enstitüsü Dergisi, 24, 672–689.
  • Postali, E., Peroukidou, P., Giaouris, E. & Papachristoforou, A. (2022). Investigating Possible Synergism in the Antioxidant and Antibacterial Actions of Honey and Propolis from the Greek Island of Samothrace through Their Combined Application. Foods, 11, 2041.
  • Ro Me Busserolles, J., Gueux, E., Rock, E., Mazur, A. & Rayssiguier, Y. (2002). Substituting Honey for Refined Carbohydrates Protects Rats from Hypertriglyceridemic and Prooxidative Effects of Fructose. The Journal of Nutrition. 132, 3379-3382.
  • Russo, N., Di Rosa, A. R., Pino, A., Mazzeo, G., Liotta, L., Caggia, C. & Randazzo, C. L. (2023). Assessment of sensory properties and in vitro antimicrobial activity of monofloral Sicilian honey. Food Bioscience, 52, 102449.
  • Segueni, N., Boutaghane, N., Asma, S. T., Tas, N., Acaroz, U., Arslan-Acaroz, D., Shah, S. R. A., Abdellatieff, H. A., Akkal, S., Peñalver, R. & Nieto, G. (2023). Review on Propolis Applications in Food Preservation and Active Packaging. Plants, 12.
  • Shah, T., Ali, N., Shah, Z. & Hayat, A. (2017). Antibacterial Activity of Pakistani Honey. Pakistan Journal of Scientific and Industrial Research Series B: Biological Sciences, 2, 97-100.
  • Shalsh, F. J., Khalaf, A. M., Hafiz, M. & Al-Sultan, I. I. A. (2021). Antibacterial Properties of Local Malaysian Trigona Sp. Honey Towards Different of Pathogenic Bacteria in vitro. Diyala Agricultural Sciences Journal, 13, 1-9.
  • Shamala, T. R., Shri Jyothi, Y. & Saibaba, P. (2000). Stimulatory effect of honey on multiplication of lactic acid bacteria under in vitro and in vivo conditions. Letters in Applied Microbiology, 30, 453–455.
  • Skadins, I., Labsvards, K. D., Grava, A., Amirian, J., Tomsone, L. E., Ruško, J., Viksna, A., Bandere, D. & Brangule, A. (2023). Antimicrobial and Antibiofilm Properties of Latvian Honey against Causative Agents of Wound Infections. Antibiotics, 12, 816.
  • Suerdem, T. B. & Akyalçın, H. (2018). Screening of antimicrobial and antioxidant activity of different types of honey samples obtained from Geyikli (Çanakkale) province. Communications Faculty of Science University of Ankara Series C Biology Geological Engineering and Geophysical Engineering, 27, 69–78.
  • Wadi, M. A. (2022). In Vitro Antibacterial Activity of Different Honey Samples against Clinical Isolates. BioMed Research International, 2022, 1-8.
  • Yılmaz, E. Ş. & Aslantaş, Ö. (2017). Antimicrobial resistance and underlying mechanisms in Staphylococcus aureus isolates. Asian Pacific Journal of Tropical Medicine, 10, 1059–1064.
  • Zapata-Vahos, I. C., Henao-Rojas, J. C., Yepes-Betancur, D. P., Marín-Henao, D., Giraldo Sánchez, C. E., Calvo-Cardona, S. J., David, D. & Quijano-Abril, M. (2023). Physicochemical Parameters, Antioxidant Capacity, and Antimicrobial Activity of Honeys from Tropical Forests of Colombia: Apis mellifera and Melipona eburnea. Foods, 12, 1001.
  • Zeaki, N., Johler, S., Skandamis, P. N. & Schelin, J. (2019). The Role of Regulatory Mechanisms and Environmental Parameters in Staphylococcal Food Poisoning and Resulting Challenges to Risk Assessment. Frontiers in Microbiology, 10, 1307.
  • Zhao, Y., Zhu, A., Tang, J., Tang, C. & Chen, J. (2017). Identification and measurement of staphylococcal enterotoxin M from Staphylococcus aureus isolate associated with staphylococcal food poisoning. Letters in Applied Microbiology, 65, 27–34.
There are 38 citations in total.

Details

Primary Language English
Subjects Veterinary Food Hygiene and Technology
Journal Section Review
Authors

Ömer Çakmak 0000-0001-7658-1284

Nuri Taş 0009-0004-7035-1444

Ulaş Acaröz 0000-0002-1533-4519

Damla Arslan-acaroz 0000-0001-9230-6725

Fatih Ramazan İstanbullugil 0000-0001-9610-2797

Sezen Evrenkaya 0000-0002-8689-234X

Zeki Gürler 0000-0002-9037-2945

Publication Date December 30, 2023
Submission Date November 4, 2023
Acceptance Date December 19, 2023
Published in Issue Year 2023 Volume: 14 Issue: 3

Cite

APA Çakmak, Ö., Taş, N., Acaröz, U., Arslan-acaroz, D., et al. (2023). INHIBITORY EFFECTS of HONEY on STAPHYLOCOCCUS AUREUS and ESCHERICHIA COLI: A CURRENT REVIEW. Veteriner Farmakoloji Ve Toksikoloji Derneği Bülteni, 14(3), 133-148. https://doi.org/10.38137/vftd.1385968

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