Open Access
Research (Published online: 29-08-2018)
26. Mixing two different propolis samples potentiates their antimicrobial activity and wound healing property: A novel approach in wound healing and infection
Noori Al-Waili
Veterinary World, 11(8): 1188-1195

Noori Al-Waili: Private Clinic, Basic Science Research, Al-Rusafa, Baghdad, Iraq; New York Medical Care for Nephrology, New York, 11418, US.

doi: 10.14202/vetworld.2018.1188-1195

Share this article on [Facebook] [LinkedIn]

Article history: Received: 08-06-2018, Accepted: 13-07-2018, Published online: 29-08-2018

Corresponding author: Noori Al-Waili


Citation: Al-Waili N (2018) Mixing two propolis samples potentiates their antimicrobial activity and wound healing properties: A novel approach in infection control and wound healing, Veterinary World, 11(8):1188-1195.

Aim: The study aimed to investigate whether mixing two different propolis samples can potentiate their biological activity. This hypothesis was tested by studying the effect of mixed propolis on microbial growth and wound healing and compared with the effect of each propolis individually.

Materials and Methods: The effect of mixing two different propolis extracts (A and B) collected from different locations in Iraq on Escherichia coli, Staphylococcus aureus, and Candida albicans was studied by minimum inhibitory concentration assessment and compared with the effect of each propolis. Wound healing effect of the mixed propolis was studied. Twenty-four rabbits were used for the experiment, and they were assigned to four groups. Wounds were created on the dorsum of each rabbit and treated by topical application of 1 mL of either mixed propolis, propolis A, or propolis B extracts or were kept without treatment as a control. Macroscopic wound evaluation was performed with an assessment of wound size, wound recovery, redness, edema, discharge, granulation tissue, and epithelialization.

Results: Propolis A was more potent than propolis B extracts to inhibit the growth of E. coli, S. aureus, and C. albicans (p<0.05). However, mixed propolis showed a higher antimicrobial activity toward all the pathogens than propolis A or propolis B extract individually (p<0.05). Furthermore, propolis A and propolis B extracts showed favorable effects on wound healing which was more pronounced with propolis A extract. Interestingly, mixed propolis accelerated wound healing faster than propolis A or propolis B extracts, and it shortened the time of reepithelialization (p<0.05).

Conclusion: This study demonstrates for the first time that mixing different propolis samples possesses a higher antimicrobial activity and higher wound healing property than individual propolis. This approach could pave the way for the development of more effective antimicrobials and wound healing agents.

Keywords: healing, microorganisms, mixed propolis, wound.


1. Kouidhi, B., Zmantar, T. and Bakhrouf, A. (2010) Anti-cariogenic and anti-biofilm activity of Tunisian propolis extract and its potential protective effect against cancer cells proliferation. Anaerobe, 16(6): 566-571. [Crossref] [PubMed]

2. Hozzein, W.N., Badr, G., Al Ghamdi, A.A., Sayed, A., Al-Waili, N.S., Garraud, O. (2015) Topical application of propolis enhance cutaneous wound healing by promoting TGF-beta/Smad-mediated collagen production in a streptozotocin-induced Type I diabetic mouse model. Cell. Physiol. Biochem., 37(3): 940-954. [Crossref] [PubMed]

3. Batista, C.M., Alves, A.V., Queiroz, L.A., Lima, B.S., Filho, R. and Araujo, A. (2018) The photoprotective and anti-inflammatory activity of red propolis extract in rats. J. Photochem. Photobiol. B, 180(3): 198-207. [Crossref] [PubMed]

4. Bhargava, P., Grover, A., Nigam, N., Kaul, A., Doi, M., Ishida, Y., Kakuta, H. and Kaul, S.C. (2018) Anticancer activity of the supercritical extract of Brazilian green propolis and its active component, artepillin C: Bioinformatics and experimental analyses of its mechanisms of action. Int. J. Oncol., 52(3): 925-932. [PubMed]

5. Rivera-Ya-ez, N., Rodriguez-Canales, M., Nieto-Ya-ez, O., Jimenez-Estrada, M., Ibarra-Barajas, M., Canales-Martinez, M.M. and Rodriguez-Monroy, M.A. (2018) Hypoglycaemic and antioxidant effects of propolis of Chihuahua in a model of experimental diabetes. Evid. Based. Complement. Alternat. Med., 11: 4360356.

6. Saito, Y., Tsuruma, K., Ichihara, K., Shimazawa, M. and Hara, H. (2015) Brazilian green propolis water extract up-regulates the early expression level of HO-1 and accelerates Nrf2 after UVA irradiation. BMC Complement. Altern. Med., 15(1): 421. [Crossref]

7. El Menyiy, N., Al Waili, N., Bakour, M., Al-Waili, H. and Lyoussi, B. (2016) Protective effect of propolis in proteinuria, crystalluria, nephrotoxicity and hepatotoxicity induced by ethylene glycol ingestion. Arch. Med. Res., 47(7): 526-534. [Crossref] [PubMed]

8. Chen, Y.W., Ye, S.R., Ting, C. and Yu, Y.H. (2018) Antibacterial activity of propolis from Taiwanese green propolis. J. Food. Drug. Anal., 26(2): 761-768. [Crossref] [PubMed]

9. Al-Waili, N., Al-Ghamdi, A., Ansari, M., Al-Attal, Y. and Salom, K. (2012) Synergistic effects of honey and propolis toward drug multi-resistant Staphylococcus aureus, Escherichia coli and Candida albicans isolates in single and polymicrobial cultures. Int. J. Med. Sci., 9(9): 793-780. [Crossref] [PubMed] [PMC]

10. Henshaw, F.R., Bolton, T., Nube, V., Hood, A., Veldhoen, D., Pfrunder, L., McKew, G.L., Macleod, C., McLennan, S.V. and Twigg, S.M. (2014) Topical application of the beehive protectant propolis is well tolerated and improves human diabetic foot ulcer healing in a prospective feasibility study. J. Diabetes Complications, 28(6): 850-857. [Crossref] [PubMed]

11. Olczyk, P., Komosinska-Vassev, K., Wisowski, G., Mencner, L., Stojko, J. and Kozma, E.M. (2014) Propolis modulates fibronectin expression in the matrix of thermal injury. Biomed. Res. Int., 2014: 748101. [Crossref] [PubMed] [PMC]

12. Machado, C.S., Mokochinski, J.B., de Lira, T.O., de Oliveira Fde, C., Cardoso, M.V. and Ferreira, R.G. (2016) Comparative study of chemical composition and biological activity of yellow, green, brown, and red Brazilian propolis. Evid. Based Complement. Alternat. Med., 2016: 6057650. [Crossref] [PubMed] [PMC]

13. Moreira, L., Dias, L.G. and Pereira, J.A. (2008) Antioxidant properties, total phenols and pollen analysis of propolis samples from Portugal. Food Chem. Toxicol., 46(11): 3482-3485. [Crossref] [PubMed]

14. Huang, S., Zhang, C., Wang, K., Li, G. and Hu, F. (2014) Recent advances in the chemical composition of Propolis. Molecules, 19: 19610-19632. [Crossref] [PubMed]

15. Kumazawa, S., Hamasaka, T. and Nakayama, T. (2004) Antioxidant activity of propolis of various geographic origins. Food. Chem., 84(3): 329-339. [Crossref]

16. Bankova, V. (2005) Chemical diversity of propolis and the problem of standardization. J. Ethnopharmacol., 100(1-2): 114-117. [Crossref] [PubMed]

17. Sforcin, J.M., Bankova, V. (2011) Propolis: Is there a potential for the development of new drugs? J. Ethnopharmacol., 133(3): 253-260. [Crossref] [PubMed]

18. Oldoni, T., Oliveira, S., Andolfatto, S., Karling, M., Calegari, M. and Sado, R. (2015) Chemical characterization and optimization of the extraction process of bioactive compounds from propolis produced by selected bees Apis mellifera. J. Braz. Chem. Soc., 26(11): 2054-2062.

19. Silici, S., Kutluca, S. (2005) Chemical composition and antibacterial activity of propolis collected by three different races of honeybees in the same region. J. Ethnopharmacol., 99(1): 69-73. [Crossref] [PubMed]

20. Seidel, V., Peyfoon, E., Watson, D. and Fearnley, J. (2008) Comparative study of the antibacterial activity of propolis from different geographical and climatic zones. Phytother. Res., 22(9): 1256-1263. [Crossref] [PubMed]

21. Bonvehi, J.S. and Gutierrez, A.L. (2012) The antimicrobial effects of propolis collected in different regions in the Basque Country (Northern Spain). World J. Microbiol. Biotechnol., 28(4): 1351-1358. [Crossref] [PubMed]

22. Dias, L.G., Pereira, A.P. and Estevinho, L.M. (2012) Comparative study of different Portuguese samples of propolis: Pollinic, sensorial, physicochemical, microbiological characterization and antibacterial activity. Food. Chem. Toxicol., 50(12): 4246-4253. [Crossref] [PubMed]

23. Touzani, S., Al-Waili, N., El Menyiy, N., Filipic, B., Pereyra, A. and EL Arabi, I. (2018) Chemical analysis and antioxidant content of various propolis samples collected from different regions and their impact on antimicrobial activities including MRSA. Asian Pac. J. Trop. Med., 11(7): 436-442.

24. Hegazi, A., Abd El Hady, F. and Abd Allah, F. (2000) Chemical composition and antimicrobial activity of European propolis. Z. Naturforsch., 55(1): 70-75. [Crossref]

25. Banskota, H., Tezuka, Y., Adnyana, K., Midorikawa, K., Matsushige, K. and Message, D. (2000) Cytotoxic, hepatoprotective and free radical scavenging effects of propolis from Brazil, Peru, the Netherlands and China. J. Ethnopharmacol., 72(1-2): 239-246. [Crossref]

26. Bryan, J., Redden, P. and Traba, C. (2016) The mechanism of action of Russian propolis ethanol extracts against two antibiotic-resistant biofilm-forming bacteria. Lett. Appl. Microbiol., 62(2): 192-198. [Crossref] [PubMed]

27. Mirzoeva, O., Grishanin, R. and Colder, P. (1997) Antimicrobial action of propolis and some of its components: The effect on growth, membrane potential and motility of bacteria. Microbiol. Res., 152(3): 239-246. [Crossref]

28. Inui, S., Hatano, A., Yoshino, M., Hosoya, T., Shimamura, Y. and Masuda, S. (2014) Identification of the phenolic compounds contributing to antibacterial activity in ethanol extracts of Brazilian red propolis. Nat. Prod. Res., 28(16): 1293-1296. [Crossref] [PubMed]

29. Veiga, R.S., De Mendonca, S., Mendes, P.B., Paulino, N., Mimica, M.J. and Netto, A.A.L. (2017) Artepillin C and phenolic compounds responsible for antimicrobial and antioxidant activity of green propolis and Baccharis dracunculifolia DC. J. Appl. Microbiol., 122(4): 911-920. [Crossref] [PubMed]

30. Al-Waili, N.S., Saloom, K.Y., Al-Waili, T., Al-Waili, A. and Al-Waili, H. (2007) Modulation of prostaglandin activity, Part 1: Prostaglandin inhibition in the management of nonrheumatologic diseases: Immunologic and hematologic aspects. Adv. Ther., 24(1): 189-222. [Crossref]

31. Larki-Harchegani, A., Hemmati, A.A., Arzi, A., Ghafurian-Boroojerdnia, M., Shabib, S., Zadkarami, M.R. and Esmaeilzadeh, S. (2013) Evaluation of the effects of caffeic acid phenethyl ester on prostaglandin E2 and two key cytokines involved in bleomycin-induced pulmonary fibrosis. Iran. J. Basic Med. Sci., 16(7): 850-857. [PubMed] [PMC]

32. Rossi, A., Longo, R., Russo, A., Borrelli, F. and Sautebin, L. (2002) The role of the phenethyl ester of caffeic acid (CAPE) in the inhibition of rat lung cyclooxygenase activity by propolis. Fitoterapia, 73 Suppl 1: S30-37. [Crossref]

33. Naito, Y., Yasumuro, M., Kondou, K. and Ohara, N. (2007) Antiinflammatory effect of topically applied propolis extract in carrageenan-induced rat hind paw edema. Phytoth. Res., 21: 452-456. [Crossref] [PubMed]

34. Funakoshi-Tago, M., Ohsawa, K., Ishikawa, T., Nakamura, F., Ueda, F. and Narukawa, Y. (2016) Inhibitory effects of flavonoids extracted from Nepalese propolis on the LPS signaling pathway. Int. Immunopharmacol., 40: 550-560. [Crossref] [PubMed]

35. Hamalainen,. M, Nieminen, R., Asmawi, M.Z., Vuorela, P., Vapaatalo, H. and Moilanen, E. (2011) Effects of flavonoids on prostaglandin E2 production and COX-2 and mPGES-1 expressions in activated macrophages. Planta. Med., 77(13): 1504-1511. [Crossref] [PubMed]

36. Correa, F., Schanuel, F.S., Moura-Nunes, N., Monte-Alto-Costa, A. and Daleprane, J.B. (2017) Brazilian red propolis improves cutaneous wound healing suppressing inflammation-associated transcription factor NF?B. Biomed. Pharmacother., 86: 162-171. [Crossref] [PubMed]

37. Miyata, S., Oda, Y., Matsuo, C., Kumura, H. and Kobayashi, K. (2014) Stimulatory effect of Brazilian propolis on hair growth through proliferation of keratinocytes in mice. J. Agric. Food Chem., 62(49): 11854-11861. [Crossref] [PubMed]

38. O'Neill, A.J. and Chopra, I. (2004) Preclinical evaluation of novel antibacterial agents by microbiological and molecular techniques. Expert. Opin. Inves. Drugs, 13(8): 1045-1063. [Crossref]