Comparison of Antimicrobial Activities of Ethanol- and Water-Based Propolis Extracts on Various Foodborne Pathogens by Agar-Well Diffusion Method

Year 2023, Volume: 54 Issue: 3 - Research in Agricultural Sciences, 130 - 136, 19.10.2023

Bahar Onaran Acar , Erman Gülendağ

https://doi.org/10.5152/AUAF.2023.23148

Abstract

Although ethanolic-based propolis extracts have been shown to have various biological activities, studies on the differences in the antimicrobial effects of water- and ethanol-based extracts, are lacking. Propolis preparations are now also sold as water-based products due to a number of factors, such as being safer for babies, being biocompatible, and some religious prohibitions on alcohol consumption. This study aimed to compare the antimicrobial effects of commercially available propolis preparations in the form of ethanol- and water-based extracts against various pathogenic microorganisms that cause foodborne infections. A total of 36 Gram-positive and Gram-negative bacterial strains from 8 different species were used in the study. As a result of the statistical analysis, only ethanol-based propolis from Turkey was effective against enterococci, Staphylococcus aureus, Bacillus cereus, Bacillus subtilis subsp. spizizenii, Salmonella spp., Listeria monocytogenes, Acinetobacter baumannii, and Pseudomonas aeroginosa, except Escherichia coli. It was concluded that the water-based extract did not have a significant inhibitory effect on the bacteria tested. It was determined that both ethanol- and water-based propolis tested in the study showed the most inhibitory effect on Acinetobacter baumannii. In addition, we can also conclude that ethanol-based propolis extract is more effective against Gram-positive bacteria than Gram-negative bacteria.

Keywords

Antimicrobial agents, antimicrobial resistance, food safety, foodborne infections, propolis

Etanol ve Su Bazlı Propolis Ekstraktlarının Çeşitli Gıda Kaynaklı Patojenler Üzerindeki Antimikrobiyal Aktivitelerinin Agar-Well Difüzyon Yöntemi ile Karşılaştırılması

Abstract

Etanol bazlı propolis ekstraktlarının çeşitli biyolojik aktivitelere sahip olduğu gösterilmiş olmasına rağmen, su ve etanol bazlı ekstraktların antimikrobiyal etkileri arasındaki farklılıklara ilişkin çalışmalar eksiktir. Propolis müstahzarları, bebekler için daha güvenli olması, biyouyumlu olması ve alkol tüketimiyle ilgili bazı dini yasaklar gibi bir dizi faktör nedeniyle artık su bazlı ürünler olarak da satılmaktadır. Bu çalışma, gıda kaynaklı infeksiyonlara neden olan çeşitli patojen mikroorganizmalara karşı etanol ve su bazlı ekstrakt formundaki ticari olarak temin edilebilen propolis preparatlarının antimikrobiyal etkilerinin karşılaştırılmasını amaçlamıştır. Çalışmada sekiz farklı soydan toplam 36 Gram pozitif ve Gram negatif bakteri suşu kullanılmıştır. İstatistiksel analizler sonucunda Türkiye'ye ait su ve alkol bazlı propolis ektraklarından sadece etanol bazlı propolisin Escherichia coli hariç, enterococci, Staphylococcus aureus, Bacillus cereus, Bacillus subtilis subsp. spizizenii, Salmonella spp., Listeria monocytogenes, Acinetobacter baumannii, and Pseudomonas aeroginosa bakterileri üzerine antimikrobiyel etki oluşturduğu tespit edilmiştir. Su bazlı ekstraktın test edilen bakteriler üzerinde önemli bir inhibitör etkiye sahip olmadığı sonucuna varılmıştır. Çalışmada test edilen etanol ve su bazlı propolislerin her ikisinin de Acinetobacter baumannii üzerinde en fazla inhibitör etki gösterdiği belirlenmiştir. Ayrıca, etanol bazlı propolis ekstraktının Gram-pozitif bakterilere karşı Gram-negatif bakteriler üzerine daha etkili olduğu sonucuna varılmıştır.

Keywords

Antimikrobiyal ajanlar, antimikrobiyal direnç, gıda güvenliği, gıda kaynaklı infeksiyonlar, propolis

References

• Afata, T. N., Nemo, R., Ishete, N., Tucho, G. T., & Dekebo, A. (2022). Phytochemical investigation, physicochemical characterization, and antimicrobial activities of Ethiopian propolis. Arabian Journal of Chemistry, 15(7), 103931. [CrossRef]
• Al-Ani, I., Zimmermann, S., Reichling, J., & Wink, M. (2018). Antimicrobial activities of European propolis collected from various geographic origins alone and in combination with antibiotics. Medicines, 5(1), 2. [CrossRef]
• Babatunde, I. R., Abdulbasit, A., Oladayo, M. I., Olasile, O. I., Olamide, F. R., & Gbolahan, B. W. (2015). Hepatoprotective and pancreatoprotective properties of the ethanolic extract of Nigerian propolis. Journal of Intercultural Ethnopharmacology, 4(2), 102–108. [CrossRef]
• Bakkaloğlu, Z., Arıcı, M., & Karasu, S. (2021). Optimization of ultrasound-assisted extraction of Turkish propolis and characterization of phenolic profile, antioxidant and antimicrobial activity. Food Science and Technology, 41(3), 687–695. [CrossRef]
• Bankova, V., Galabov, A. S., Antonova, D., Vilhelmova, N., & Di Perri, B. (2014). Chemical composition of Propolis Extract ACF® and activity against herpes simplex virus. Phytomedicine, 21(11), 1432–1438. [CrossRef]
• Bankova, V., Popova, M., Bogdanov, S., & Sabatini, A. G. (2002). Chemical composition of European propolis: Expected and unexpected results. Zeitschrift Fur Naturforschung. C, Journal of Biosciences, 57(5–6), 530–533. [CrossRef]
• Bilir Ormancı, F. S., Erol, I., Ayaz, N. D., İşeri, O., & Sarıgüzel, D. (2008). Immunomagnetic separation and PCR detection of Listeria monocytogenes in turkey meat and antibiotic resistance of the isolates. British Poultry Science, 49(5), 560–565. [CrossRef]
• Boyanova, L., Gergova, G., Nikolov, R., Derejian, S., Lazarova, E., Katsarov, N., Mitov, I., & Krastev, Z. (2005). Activity of Bulgarian propolis against 94 Helicobacter pylori strains in vitro by agar-well diffusion, agar dilution and disc diffusion methods. Journal of Medical Microbiology, 54(5), 481–483. [CrossRef]
• Centers for Disease Control and Prevention (CDC). (2019). Antibiotic resistance threats in the United States. https://www.cdc.gov/drugresistance/pdf/threats-report/2019-ar-threats-report-508.pdf
• Chan, G. C. F., Cheung, K. W., & Sze, D. M. Y. (2013). The immunomodulatory and anticancer properties of propolis. Clinical Reviews in Allergy and Immunology, 44(3), 262–273. [CrossRef]
• da Silva, S. S., Mizokami, S. S., Fanti, J. R., Miranda, M. M., Kawakami, N. Y., Teixeira, F. H., Araújo, E. J. A., Panis, C., Watanabe, M. A. E., Sforcin, J. M., Pavanelli, W. R., Verri Jr., W. A., Felipe, I., & Conchon-Costa, I. (2016). Propolis reduces Leishmania amazonensis-induced inflammation in the liver of BALB/c mice. Parasitology Research, 115(4), 1557–1566. [CrossRef]
• Dos Santos, C. M., de Souza Mesquita, L. M., Braga, A. R. C., & De Rosso, V. V. (2021). Red propolis as a source of antimicrobial phytochemicals: Extraction using high-performance alternative solvents. Frontiers in Microbiology, 12, 659911. [CrossRef]
• Freitas, A. S., Cunha, A., Oliveira, R., & Almeida‐Aguiar, C. (2022). Propolis antibacterial and antioxidant synergisms with gentamicin and honey. Journal of Applied Microbiology, 132(4), 2733–2745. [CrossRef]
• Fung, F., Wang, H. S., & Menon, S. (2018). Food safety in the 21st century. Biomedical Journal, 41(2), 88–95. [CrossRef]
• Gao, W., Wu, J., Wei, J., Pu, L., Guo, C., Yang, J., Yang, M., & Luo, H. (2014). Brazilian green propolis improves immune function in aged mice. Journal of Clinical Biochemistry and Nutrition, 55(1), 7–10. [CrossRef]
• Garzoli, S., Maggio, F., Vinciguerra, V., Rossi, C., Donadu, M. G., & Serio, A. (2023). Chemical characterization and antimicrobial properties of the hydroalcoholic solution of Echinacea purpurea (L.) Moench and propolis from Northern Italy. Molecules, 28(3), 1380. [CrossRef]
• Gummuluri, S., Kavalipurapu, V. T., & Kaligotla, A. V. (2019). Antimicrobial efficacy of novel ethanolic extract of Morinda citrifolia against Enterococcus feacalis by agar well diffusion method and minimal ınhibitory concentration-An invitro study. Brazilian Dental Science, 22(3), 365–370. [CrossRef]
• Hannan, A., Batool, A., Qamar, M. U., & Khalid, F. (2015). Propolis as an antibacterial agent against clinical isolates of MDR-Acinetobacter baumannii. Journal of Ayub Medical College, Abbottabad, 27(1), 216–219.
• Hegazi, A. G., Abd El Hady, F. K., & Abd Allah, F. A. (2000). Chemical composition and antimicrobial activity of European propolis. Zeitschrift Fur Naturforschung. C, Journal of iosciences, 55(1–2), 70–75. [CrossRef]
• Hori, J. I., Zamboni, D. S., Carrão, D. B., Goldman, G. H., & Berretta, A. A. (2013). The inhibition of inflammasome by Brazilian propolis (EPPAF). Evidence-Based Complementary and alternative Medicine: eCAM, 2013, 418508. [CrossRef]
• Huang, S., Zhang, C. P., Wang, K., Li, G. Q., & Hu, F. L. (2014). Recent advances in the chemical composition of propolis. Molecules, 19(12), 19610–19632. [CrossRef]
• Huemer, M., Mairpady Shambat, S., Brugger, S. D., & Zinkernagel, A. S. (2020). Antibiotic resistance and persistence—Implications for human health and treatment perspectives. EMBO Reports, 21(12), e51034. [CrossRef]
• Hutchings, M. I., Truman, A. W., & Wilkinson, B. (2019). Antibiotics: Past, present and future. Current Opinion in Microbiology, 51, 72–80. [CrossRef]
• Hünler Dönmez, İ. (2021). Doğal kaynaklı ürünlerin oral patojenler üzerinde antimikrobiyal etkinliklerinin in vitro değerlendirilmesi (Doktora tezi, Tez no: 10431839). GAZİ ünİversİtesİ sağlik bİlİmlerİ enstİtüsü. https://avesis.gazi.edu.tr/dosya?id=329e5435-d277-4464-aa2e-ab83702e4dcf
• Kim, M. J., Kim, C. S., Kim, B. H., Ro, S. B., Lim, Y. K., Park, S. N., Cho, E., Ko, J. H., Kwon, S. S., Ko, Y. M., & Kook, J. K. (2011). Antimicrobial effect of Korean propolis against the mutans treptococci isolated from Korean. Journal of Microbiology, 49(1), 161–164. [CrossRef]
• Massaro, C. F., Simpson, J. B., Powell, D., & Brooks, P. (2015). Chemical composition and antimicrobial activity of honeybee (Apis mellifera ligustica) propolis from subtropical eastern Australia. Science of Nature, 102, 1–11. [CrossRef]
• Mavri, A., Abramovič, H., Polak, T., Bertoncelj, J., Jamnik, P., Smole Možina, S., & Jeršek, B. (2012). Chemical properties and antioxidant and antimicrobial activities of Slovenian propolis. Chemistry and Biodiversity, 9(8), 1545–1558. [CrossRef]
• Morehead, M. S., & Scarbrough, C. (2018). Emergence of global antibiotic resistance. Primary Care, 45(3), 467–484. [CrossRef]
• Ömer, H. H. S., Demirtaş, I., & Özen, T. (2023). Investigation of phenolic contents and bioactivities of water-based extracts prepared from cryogenically pulverized Turkish propolis. Journal of Food Measurement and Characterization, 17(2), 1586–1601. [CrossRef]
• Pires, S. M., Desta, B. N., Mughini-Gras, L., Mmbaga, B. T., Fayemi, O. E., Salvador, E. M., Gobena, T., Majowicz, S. E., Hald, T., Hoejskov, P. S., Minato, Y., & Devleesschauwer, B. (2021). Burden of foodborne diseases: Think global, act local. Current Opinion in Food Science, 39, 152–159. [CrossRef]
• Pisoschi, A. M., Pop, A., Georgescu, C., Turcuş, V., Olah, N. K., & Mathe, E. (2018). An overview of natural antimicrobials role in food. European Journal of Medicinal Chemistry, 143, 922–935. [CrossRef]
• Pobiega, K., Kraśniewska, K., Derewiaka, D., & Gniewosz, M. (2019). Comparison of the antimicrobial activity of propolis extracts obtained by means of various extraction methods. Journal of Food Science and Technology, 56(12), 5386–5395. [CrossRef]
• Popova, M., Dimitrova, R., Al-Lawati, H. T., Tsvetkova, I., Najdenski, H., & Bankova, V. (2013). Omani propolis: Chemical profiling, antibacterial activity and new propolis plant sources. Chemistry Central Journal, 7(1), 158. [CrossRef]
• 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 Samo Thrace through their combined application. Foods, 11(14), 2041. [CrossRef]
• Przybyłek, I., & Karpiński, T. M. (2019). Antibacterial properties of propolis. Molecules, 24(11), 2047. [CrossRef]
• Ramirez, J., Guarner, F., Bustos Fernandez, L., Maruy, A., Sdepanian, V. L., & Cohen, H. (2020). Antibiotics as major disruptors of gut microbiota. Frontiers in Cellular and Infection Microbiology, 10, 572912. [CrossRef]
• Rendueles, E., Mauriz, E., Sanz-Gómez, J., Adanero-Jorge, F., & GarcíaFernandez, C. (2023). Antimicrobial activity of Spanish propolis against Listeria monocytogenes and other listeria strains. Microorganisms, 11(6), 1429. [CrossRef]
• Santos, L. M., Fonseca, M. S., Sokolonski, A. R., Deegan, K. R., Araújo, R. P., Umsza‐Guez, M. A., Barbosa, J. D., Portela, R. D., & Machado, B. A. (2020). Propolis: Types, composition, biological activities, and veterinary product patent prospecting. Journal of the Science of Food and Agriculture, 100(4), 1369–1382. [CrossRef]
• Stepanović, S., Antić, N., Dakić, I., & Švabić-Vlahović, M. (2003). In vitro antimicrobial activity of propolis and synergism between propolis and antimicrobial drugs. Microbiological Research, 158(4), 353–357. [CrossRef]
• Touzani, S., Imtara, H., Katekhaye, S., Mechchate, H., Ouassou, H., Alqahtani, A. S., Noman, O. M., Nasr, F. A., Fearnley, H., Fearnley, J., Paradkar, A., ElArabi, I., & Lyoussi, B. (2021). Determination of phenolic compounds in various propolis samples collected from an African and an Asian region and their impact on antioxidant and antibacterial activities. Molecules, 26(15), 4589. [CrossRef]
• Uzel, A., Sorkun, K., Onçağ, O., Cogŭlu, D., Gençay, O., & Salih, B. (2005). Chemical compositions and antimicrobial activities of four different Anatolian propolis samples. Microbiological Research, 160(2), 189–195. [CrossRef]
• Velikova, M., Bankova, V., Sorkun, K., Houcine, S., Tsvetkova, I., & Kujumgiev, A. (2000). Propolis from the Mediterranean region: Chemical composition and antimicrobial activity. Zeitschrift Fur Naturforschung. C, Journal of Biosciences, 55(9–10), 790–793. [CrossRef]
• Zhao, L., Pu, L., Wei, J., Li, J., Wu, J., Xin, Z., Gao, W., & Guo, C. (2016). Brazilian green propolis improves antioxidant function in patients with type 2 diabetes mellitus. International Journal of Environmental Research and Public Health, 13(5), 498. [CrossRef]