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Synergistic interaction between propolis extract, essential oils, and antibiotics against Staphylococcus epidermidis and methicillin resistant Staphylococcus aureus

Year 2021, Volume 8, Issue 3, 195 - 213, 10.09.2021
https://doi.org/10.21448/ijsm.947033

Abstract

The development of multi-drug-resistant bacteria pushed the scientific community to look for new alternatives to solve the problem. Propolis is a beehive substance and one of the richest natural products in bioactive compounds with antibacterial activity. This study was aimed to investigate the possible synergistic interaction between propolis and antibacterial drugs, such as essential oils (EOs) and antibiotics, in order to find increased activity with decreased concentrations. Two ethanol extracts of propolis were used for the test, which were collected from the north of Morocco. The chemical composition was determined by UHPLC-MS. The synergistic effect of propolis extracts with EOs and antibiotics was tested using the checkerboard technique. The chemical analysis showed the presence of more that 100 compounds in propolis extracts, belonging mainly to flavonoids. The combination of propolis with the other antibacterial drugs showed different types of interactions with FIC index values varied from 0.18 to 1, but no antagonist effect was noticed. With FICI<0.5, the synergistic effect was obtained with essential oils as well as with antibiotics. These results indicate that propolis can be a promising source of molecules with medical interest to treat bacterial infection and/or to increase the action of antibiotics.

References

  • Bankova, V., Popova, M., & Trusheva, B. (2014). Propolis volatile compounds: Chemical diversity and biological activity: A review. Chemistry Central Journal, 8(1), 28. https://doi.org/10.1186/1752-153X-8-28
  • Bantar, C., Vesco, E., Heft, C., Salamone, F., Krayeski, M., Gomez, H., Coassolo, M. A., Fiorillo, A., Franco, D., Arango, C., Duret, F., & Oliva, M. E. (2004). Replacement of broad-spectrum cephalosporins by piperacillin-tazobactam: Impact on sustained high rates of bacterial resistance. Antimicrob. Agents Chemother., 48(2), 392 395. https://doi.org/10.1128/aac.48.2.392-395.2004
  • Bouhdid, S., Abrini, J., Zhiri, A., Espuny, M. J., & Manresa, A. (2009). Investigation of functional and morphological changes in Pseudomonas aeruginosa and Staphylococcus aureus cells induced by Origanum compactum essential oil. J. Appl. Microbiol., 106(5), 1558-1568. https://doi.org/10.1111/j.1365-2672.2008.04124.x
  • Bouyahya, A., Abrini, J., Et-Touys, A., Bakri, Y., & Dakka, N. (2017). Indigenous knowledge of the use of medicinal plants in the North-West of Morocco and their biological activities. European Journal of Integrative Medicine, 13, 9-25.
  • Denes, É., & Hidri, N. (2009). Synergie et antagonisme en antibiothérapie. Antibiotiques, 11(2), 106-115. https://doi.org/10.1016/j.antib.2009.02.001
  • Fernandes Júnior, A., Balestrin, E. C., Betoni, J. E. C., Orsi, R. de O., Cunha, M. de L. R. de S. da, & Montelli, A. C. (2005). Propolis: Anti-Staphylococcus aureus activity and synergism with antimicrobial drugs. Memórias Do Instituto Oswaldo Cruz, 100(5), 563-566. https://doi.org/10.1590/S0074-02762005000500018
  • Ghisalberti, E. L. (1979). Propolis: A Review. Bee World, 60(2), 59 84. https://doi.org/10.1080/0005772X.1979.11097738
  • Guz, N. R., Stermitz, F. R., Johnson, J. B., Beeson, T. D., Willen, S., Hsiang, J.-F., & Lewis, K. (2001). Flavonolignan and Flavone Inhibitors of a Staphylococcus a ureus Multidrug Resistance Pump: Structure−Activity Relationships. J. Med. Chem., 44(2), 261-268. https://doi.org/10.1021/jm0004190
  • Hegazi, A. G., Abd El Hady, F. K., & Abd Allah, F. A. M. (2000). Chemical Composition and Antimicrobial Activity of European Propolis. Zeitschrift Für Naturforschung C, 55(1-2), 70-75. https://doi.org/10.1515/znc-2000-1-214
  • Hirai, I., Okuno, M., Katsuma, R., Arita, N., Tachibana, M., & Yamamoto, Y. (2010). Characterisation of anti-Staphylococcus aureus activity of quercetin: Anti-MRSA activity of quercetin. International J. Food Sci. Technol., 45(6), 1250 1254. https://doi.org/10.1111/j.1365-2621.2010.02267.x
  • Huang, S., Zhang, C.-P., Wang, K., Li, G., & Hu, F.-L. (2014). Recent Advances in the Chemical Composition of Propolis. Molecules, 19(12), 19610 19632. https://doi.org/10.3390/molecules191219610
  • Krol, W., Scheller, S., Shani, J., Pietsz, G., & Czuba, Z. (1993). Synergistic effect of ethanolic extract of propolis and antibiotics on the growth of staphylococcus aureus. Arzneimittel-Forschung, 43(5), 607-609. https://europepmc.org/article/med/8329008
  • Kuropatnicki, A. K., Szliszka, E., & Krol, W. (2013). Historical Aspects of Propolis Research in Modern Times. Evid. Based Complement. Alternat. Med, 2013, 1 11. https://doi.org/10.1155/2013/964149
  • Kwon, M. J., Shin, H. M., Perumalsamy, H., Wang, X., & Ahn, Y.-J. (2020). Antiviral effects and possible mechanisms of action of constituents from Brazilian propolis and related compounds. J. Apicult. Res., 59(4), 413 425. https://doi.org/10.1080/00218839.2019.1695715
  • Lambert, R. J. W., Skandamis, P. N., Coote, P. J., & Nychas, G.-J. E. (2001). A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J. Appl. Microbiol., 91(3), 453-462. https://doi.org/10.1046/j.1365-2672.2001.01428.x
  • Lu, L.-C., Chen, Y.-W., & Chou, C.-C. (2005). Antibacterial activity of propolis against Staphylococcus aureus. International J. Food Microbiol., 102(2), 213 220. https://doi.org/10.1016/j.ijfoodmicro.2004.12.017
  • Mohamadi, N., Sharififar, F., Pournamdari, M., & Ansari, M. (2018). A Review on Biosynthesis, Analytical Techniques, and Pharmacological Activities of Trigonelline as a Plant Alkaloid. J. Dietary Suppl., 15(2), 207 222. https://doi.org/10.1080/19390211.2017.1329244
  • Orsatti, C. L., Missima, F., Pagliarone, A. C., Bachiega, T. F., Búfalo, M. C., Araújo, J. P., & Sforcin, J. M. (2010). Propolis immunomodulatory action in vivo on Toll-like receptors 2 and 4 expression and on pro-inflammatory cytokines production in mice: propolis action on toll like receptors and cytokines. Phytother. Res., 24(8), 1141 1146. https://doi.org/10.1002/ptr.3086
  • Rivero-Cruz, J. F., Granados-Pineda, J., Pedraza-Chaverri, J., Pérez-Rojas, J. M., Kumar-Passari, A., Diaz-Ruiz, G., & Rivero-Cruz, B. E. (2020). Phytochemical Constituents, Antioxidant, Cytotoxic, and Antimicrobial Activities of the Ethanolic Extract of Mexican Brown Propolis. Antioxidants, 9(1), 70. https://doi.org/10.3390/antiox9010070
  • Salatino, A., Fernandes-Silva, C. C., Righi, A. A., & Salatino, M. L. F. (2011). Propolis research and the chemistry of plant products. Nat. Prod. Rep., 28(5), 925. https://doi.org/10.1039/c0np00072h
  • Sforcin, J. M., Fernandes, A., Lopes, C. A. M., Bankova, V., & Funari, S. R. C. (2000). Seasonal effect on Brazilian propolis antibacterial activity. J. Ethnopharmacol., 73(1), 243-249. https://doi.org/10.1016/S0378-8741(00)00320-2
  • Šturm, L., & Ulrih, N. P. (2019). Advances in the Propolis Chemical Composition between 2013 and 2018: A Review. EFood, 1(1), 24. https://doi.org/10.2991/efood.k.191029.001
  • Ultee, A., Bennik, M. H. J., & Moezelaar, R. (2002). The Phenolic Hydroxyl Group of Carvacrol Is Essential for Action against the Food-Borne Pathogen Bacillus cereus. Appl. Environmen. Microbiol., 68(4), 1561-1568. https://doi.org/10.1128/AEM.68.4.1561-1568.2002
  • Ventola, C.L (2015) The Antibiotic Resistance Crisis: Part 1—Causes and Threats. Pharmacy and Therapeutics, 40, 277-283.
  • Wu, D., Kong, Y., Han, C., Chen, J., Hu, L., Jiang, H., & Shen, X. (2008). D-Alanine:d-alanine ligase as a new target for the flavonoids quercetin and apigenin. Int. J. Antimicro. Agent., 32(5), 421-426. https://doi.org/10.1016/j.ijantimicag.2008.06.010
  • Xu, J., Zhou, F., Ji, B.-P., Pei, R.-S., & Xu, N. (2008). The antibacterial mechanism of carvacrol and thymol agains Escherichia coli. Lett. Appl. Microbiol., 47(3), 174 179. https://doi.org/10.1111/j.1472-765X.2008.02407.x
  • Yousif, L., Belmehdi, O., Abdelhakim, B., Skali Senhaji, N., & Abrini, J. (2020). Does the domestication of Origanum compactum (Benth) affect its chemical composition and antibacterial activity? Flavour and Fragrance Journal, 36(2), 264 271. https://doi.org/10.1002/ffj.3641
  • Zengin, G., Uysal, A., Diuzheva, A., Gunes, E., Jekő, J., Cziáky, Z., Picot-Allain, C. M. N., & Mahomoodally, M. F. (2018). Characterization of phytochemical components of Ferula halophila extracts using HPLC-MS/MS and their pharmacological potentials: A multi-functional insight. J. Pharm. Biomed. Anal., 160, 374 382. https://doi.org/10.1016/j.jpba.2018.08.020
  • Zhou, J., Chan, L., & Zhou, S. (2012). Trigonelline: A Plant Alkaloid with Therapeutic Potential for Diabetes and Central Nervous System Disease. Curr. Med. Chem., 19(21), 3523-3531. https://doi.org/10.2174/092986712801323171

Synergistic interaction between propolis extract, essential oils, and antibiotics against Staphylococcus epidermidis and methicillin resistant Staphylococcus aureus

Year 2021, Volume 8, Issue 3, 195 - 213, 10.09.2021
https://doi.org/10.21448/ijsm.947033

Abstract

The development of multi-drug-resistant bacteria pushed the scientific community to look for new alternatives to solve the problem. Propolis is a beehive substance and one of the richest natural products in bioactive compounds with antibacterial activity. This study was aimed to investigate the possible synergistic interaction between propolis and antibacterial drugs, such as essential oils (EOs) and antibiotics, in order to find increased activity with decreased concentrations. Two ethanol extracts of propolis were used for the test, which were collected from the north of Morocco. The chemical composition was determined by UHPLC-MS. The synergistic effect of propolis extracts with EOs and antibiotics was tested using the checkerboard technique. The chemical analysis showed the presence of more that 100 compounds in propolis extracts, belonging mainly to flavonoids. The combination of propolis with the other antibacterial drugs showed different types of interactions with FIC index values varied from 0.18 to 1, but no antagonist effect was noticed. With FICI<0.5, the synergistic effect was obtained with essential oils as well as with antibiotics. These results indicate that propolis can be a promising source of molecules with medical interest to treat bacterial infection and/or to increase the action of antibiotics.

References

  • Bankova, V., Popova, M., & Trusheva, B. (2014). Propolis volatile compounds: Chemical diversity and biological activity: A review. Chemistry Central Journal, 8(1), 28. https://doi.org/10.1186/1752-153X-8-28
  • Bantar, C., Vesco, E., Heft, C., Salamone, F., Krayeski, M., Gomez, H., Coassolo, M. A., Fiorillo, A., Franco, D., Arango, C., Duret, F., & Oliva, M. E. (2004). Replacement of broad-spectrum cephalosporins by piperacillin-tazobactam: Impact on sustained high rates of bacterial resistance. Antimicrob. Agents Chemother., 48(2), 392 395. https://doi.org/10.1128/aac.48.2.392-395.2004
  • Bouhdid, S., Abrini, J., Zhiri, A., Espuny, M. J., & Manresa, A. (2009). Investigation of functional and morphological changes in Pseudomonas aeruginosa and Staphylococcus aureus cells induced by Origanum compactum essential oil. J. Appl. Microbiol., 106(5), 1558-1568. https://doi.org/10.1111/j.1365-2672.2008.04124.x
  • Bouyahya, A., Abrini, J., Et-Touys, A., Bakri, Y., & Dakka, N. (2017). Indigenous knowledge of the use of medicinal plants in the North-West of Morocco and their biological activities. European Journal of Integrative Medicine, 13, 9-25.
  • Denes, É., & Hidri, N. (2009). Synergie et antagonisme en antibiothérapie. Antibiotiques, 11(2), 106-115. https://doi.org/10.1016/j.antib.2009.02.001
  • Fernandes Júnior, A., Balestrin, E. C., Betoni, J. E. C., Orsi, R. de O., Cunha, M. de L. R. de S. da, & Montelli, A. C. (2005). Propolis: Anti-Staphylococcus aureus activity and synergism with antimicrobial drugs. Memórias Do Instituto Oswaldo Cruz, 100(5), 563-566. https://doi.org/10.1590/S0074-02762005000500018
  • Ghisalberti, E. L. (1979). Propolis: A Review. Bee World, 60(2), 59 84. https://doi.org/10.1080/0005772X.1979.11097738
  • Guz, N. R., Stermitz, F. R., Johnson, J. B., Beeson, T. D., Willen, S., Hsiang, J.-F., & Lewis, K. (2001). Flavonolignan and Flavone Inhibitors of a Staphylococcus a ureus Multidrug Resistance Pump: Structure−Activity Relationships. J. Med. Chem., 44(2), 261-268. https://doi.org/10.1021/jm0004190
  • Hegazi, A. G., Abd El Hady, F. K., & Abd Allah, F. A. M. (2000). Chemical Composition and Antimicrobial Activity of European Propolis. Zeitschrift Für Naturforschung C, 55(1-2), 70-75. https://doi.org/10.1515/znc-2000-1-214
  • Hirai, I., Okuno, M., Katsuma, R., Arita, N., Tachibana, M., & Yamamoto, Y. (2010). Characterisation of anti-Staphylococcus aureus activity of quercetin: Anti-MRSA activity of quercetin. International J. Food Sci. Technol., 45(6), 1250 1254. https://doi.org/10.1111/j.1365-2621.2010.02267.x
  • Huang, S., Zhang, C.-P., Wang, K., Li, G., & Hu, F.-L. (2014). Recent Advances in the Chemical Composition of Propolis. Molecules, 19(12), 19610 19632. https://doi.org/10.3390/molecules191219610
  • Krol, W., Scheller, S., Shani, J., Pietsz, G., & Czuba, Z. (1993). Synergistic effect of ethanolic extract of propolis and antibiotics on the growth of staphylococcus aureus. Arzneimittel-Forschung, 43(5), 607-609. https://europepmc.org/article/med/8329008
  • Kuropatnicki, A. K., Szliszka, E., & Krol, W. (2013). Historical Aspects of Propolis Research in Modern Times. Evid. Based Complement. Alternat. Med, 2013, 1 11. https://doi.org/10.1155/2013/964149
  • Kwon, M. J., Shin, H. M., Perumalsamy, H., Wang, X., & Ahn, Y.-J. (2020). Antiviral effects and possible mechanisms of action of constituents from Brazilian propolis and related compounds. J. Apicult. Res., 59(4), 413 425. https://doi.org/10.1080/00218839.2019.1695715
  • Lambert, R. J. W., Skandamis, P. N., Coote, P. J., & Nychas, G.-J. E. (2001). A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J. Appl. Microbiol., 91(3), 453-462. https://doi.org/10.1046/j.1365-2672.2001.01428.x
  • Lu, L.-C., Chen, Y.-W., & Chou, C.-C. (2005). Antibacterial activity of propolis against Staphylococcus aureus. International J. Food Microbiol., 102(2), 213 220. https://doi.org/10.1016/j.ijfoodmicro.2004.12.017
  • Mohamadi, N., Sharififar, F., Pournamdari, M., & Ansari, M. (2018). A Review on Biosynthesis, Analytical Techniques, and Pharmacological Activities of Trigonelline as a Plant Alkaloid. J. Dietary Suppl., 15(2), 207 222. https://doi.org/10.1080/19390211.2017.1329244
  • Orsatti, C. L., Missima, F., Pagliarone, A. C., Bachiega, T. F., Búfalo, M. C., Araújo, J. P., & Sforcin, J. M. (2010). Propolis immunomodulatory action in vivo on Toll-like receptors 2 and 4 expression and on pro-inflammatory cytokines production in mice: propolis action on toll like receptors and cytokines. Phytother. Res., 24(8), 1141 1146. https://doi.org/10.1002/ptr.3086
  • Rivero-Cruz, J. F., Granados-Pineda, J., Pedraza-Chaverri, J., Pérez-Rojas, J. M., Kumar-Passari, A., Diaz-Ruiz, G., & Rivero-Cruz, B. E. (2020). Phytochemical Constituents, Antioxidant, Cytotoxic, and Antimicrobial Activities of the Ethanolic Extract of Mexican Brown Propolis. Antioxidants, 9(1), 70. https://doi.org/10.3390/antiox9010070
  • Salatino, A., Fernandes-Silva, C. C., Righi, A. A., & Salatino, M. L. F. (2011). Propolis research and the chemistry of plant products. Nat. Prod. Rep., 28(5), 925. https://doi.org/10.1039/c0np00072h
  • Sforcin, J. M., Fernandes, A., Lopes, C. A. M., Bankova, V., & Funari, S. R. C. (2000). Seasonal effect on Brazilian propolis antibacterial activity. J. Ethnopharmacol., 73(1), 243-249. https://doi.org/10.1016/S0378-8741(00)00320-2
  • Šturm, L., & Ulrih, N. P. (2019). Advances in the Propolis Chemical Composition between 2013 and 2018: A Review. EFood, 1(1), 24. https://doi.org/10.2991/efood.k.191029.001
  • Ultee, A., Bennik, M. H. J., & Moezelaar, R. (2002). The Phenolic Hydroxyl Group of Carvacrol Is Essential for Action against the Food-Borne Pathogen Bacillus cereus. Appl. Environmen. Microbiol., 68(4), 1561-1568. https://doi.org/10.1128/AEM.68.4.1561-1568.2002
  • Ventola, C.L (2015) The Antibiotic Resistance Crisis: Part 1—Causes and Threats. Pharmacy and Therapeutics, 40, 277-283.
  • Wu, D., Kong, Y., Han, C., Chen, J., Hu, L., Jiang, H., & Shen, X. (2008). D-Alanine:d-alanine ligase as a new target for the flavonoids quercetin and apigenin. Int. J. Antimicro. Agent., 32(5), 421-426. https://doi.org/10.1016/j.ijantimicag.2008.06.010
  • Xu, J., Zhou, F., Ji, B.-P., Pei, R.-S., & Xu, N. (2008). The antibacterial mechanism of carvacrol and thymol agains Escherichia coli. Lett. Appl. Microbiol., 47(3), 174 179. https://doi.org/10.1111/j.1472-765X.2008.02407.x
  • Yousif, L., Belmehdi, O., Abdelhakim, B., Skali Senhaji, N., & Abrini, J. (2020). Does the domestication of Origanum compactum (Benth) affect its chemical composition and antibacterial activity? Flavour and Fragrance Journal, 36(2), 264 271. https://doi.org/10.1002/ffj.3641
  • Zengin, G., Uysal, A., Diuzheva, A., Gunes, E., Jekő, J., Cziáky, Z., Picot-Allain, C. M. N., & Mahomoodally, M. F. (2018). Characterization of phytochemical components of Ferula halophila extracts using HPLC-MS/MS and their pharmacological potentials: A multi-functional insight. J. Pharm. Biomed. Anal., 160, 374 382. https://doi.org/10.1016/j.jpba.2018.08.020
  • Zhou, J., Chan, L., & Zhou, S. (2012). Trigonelline: A Plant Alkaloid with Therapeutic Potential for Diabetes and Central Nervous System Disease. Curr. Med. Chem., 19(21), 3523-3531. https://doi.org/10.2174/092986712801323171

Details

Primary Language English
Subjects Biology
Published Date September
Journal Section Articles
Authors

Omar BELMEHDİ This is me
Abdelmalek Essaadi university
0000-0000-0000-0000
Morocco


Abdelhakim BOUYAHYA This is me
Mohammed V University of Rabat
0000-0001-9317-1631
Morocco


József JEKŐ This is me
University of Nyíregyháza
0000-0001-5594-6870
Hungary


Zoltán CZİÁKY This is me
University of Nyíregyháza
0000-0002-1846-3236
Hungary


Gokhan ZENGİN (Primary Author)
Selçuk Üniversitesi
0000-0001-6548-7823
Türkiye


Gyula SOTKÓ This is me
0000-0001-9894-7216
Hungary


Aicha EL BAABOUA This is me
Abdelmalek Essaadi university
0000-0002-3048-5390
Morocco


Nadia Skali SENHAJİ This is me
Abdelmalek Essaadi university
0000-0002-7356-1648
Morocco


Jamal ABRİNİ This is me
Abdelmalek Essaadi university
0000-0002-5103-9365
Morocco

Publication Date September 10, 2021
Published in Issue Year 2021, Volume 8, Issue 3

Cite

APA Belmehdi, O. , Bouyahya, A. , Jekő, J. , Cziáky, Z. , Zengin, G. , Sotkó, G. , El Baaboua, A. , Senhaji, N. S. & Abrini, J. (2021). Synergistic interaction between propolis extract, essential oils, and antibiotics against Staphylococcus epidermidis and methicillin resistant Staphylococcus aureus . International Journal of Secondary Metabolite , 8 (3) , 195-213 . DOI: 10.21448/ijsm.947033

International Journal of Secondary Metabolite (IJSM)

ISSN-e: 2148-6905