Research Article
Moroccan Propolis: A Natural Antioxidant, Antibacterial, and
Antibiofilm against Staphylococcus aureus with No Induction of
Resistance after Continuous Exposure
Souka\na El-Guendouz ,
1,2
Smail Aazza,
1,2
Badiaa Lyoussi ,
1
Vassya Bankova ,
3
Milena Popova,
3
Lu-s Neto,
4
Maria Leonor Faleiro,
5
and Maria da Graça Miguel
2
1
Laboratory of Physiology-Pharmacology-Environmental Health, Faculty of Sciences Dhar El Mehraz, BP 1796 Atlas,
University Sidi Mohamed Ben Abdallah, Fez 30 000, Morocco
2
Department of Chemistry and Pharmacy, Faculty of Science and Technology, University of Algarve, Campus de Gambelas,
MeditBio, 8005-139 Faro, Portugal
3
Institute of Organic Chemistry with Centre of Phytochemistry, Acad. G. Bonchev Strl. Bl. 9, 1113 Sofa, Bulgaria
4
Department of Biological Sciences and Bioengineering, Faculty of Science and Technology, University of Algarve,
Campus de Gambelas, 8005-139 Faro, Portugal
5
Department of Biological Sciences and Bioengineering, Faculty of Science and Technology,
Center for Biomedical Research University of Algarve, Campus de Gambelas, 8005-139 Faro, Portugal
Correspondence should be addressed to Maria da Grac ¸a Miguel; mgmiguel@ualg.pt
Received 20 July 2018; Revised 26 September 2018; Accepted 2 October 2018; Published 12 November 2018
Academic Editor: Jos´ e L. Rios
Copyright © 2018 Souka¨ ına El-Guendouz et al. Tis is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
Tis study was performed to evaluate the total phenols, favonoids, and antioxidant activities of twenty-four propolis samples from
diferent regions of Morocco. In addition, two samples were screened regarding the antibacterial efect against four Staphylococcus
aureus strains. Gas chromatography coupled to mass spectra (GC-MS) analysis was done for propolis samples used in antibacterial
tests. Te minimum inhibitory and minimum bactericidal concentration (MIC, MBC) were determined. Te potential to acquire
the resistance afer sequential exposure of bacterial strains and the impact of adaptation to propolis on virulence using the Galleria
mellonella were evaluated. Additionally, the efects of propolis extract on the bacterial adherence ability and its ability to inhibit the
quorum sensing activity were also examined. Among the twenty-four extracts studied, the samples from Sefrou, Outat el Haj, and
the two samples marketed in Morocco were the best for scavenging DPPH, ABTS, NO, peroxyl, and superoxide radicals as well as
in scavenging of hydrogen peroxide. A strong correlation was found between the amounts of phenols, favonoids, and antioxidant
activities. Propolis extract at the MIC value (0.36 mg/mL) signifcantly reduced (p < 0.001) the virulence potential of S. aureus ATCC
6538 and the MRSA strains without leading to the development of resistance in the sequence of continuous exposure. It was able
to impair the bacterial bioflm formation. Te results have revealed that sample 1 reduces violacein production in a concentration
dependent manner, indicating inhibition of quorum sensing. Tis extract has as main group of secondary metabolites favonoids
(31.9%), diterpenes (21.5%), and phenolic acid esters (16.5%).
1. Introduction
Reactive oxygen species (ROS) have a dual role in living
beings. In adequate concentrations, they have a benefcial
efect because they may constitute as defense against infec-
tious agents, or being involved in some cellular signaling
systems. Nevertheless, at higher concentrations, they damage
cell structures (membranes) and biomolecules (lipids, nucleic
acids, and proteins), leading to the known oxidative stress and
consequently to the development of several age-dependent
diseases (cancer, arteriosclerosis, arthritis, and neurode-
generative diseases, among others) [1]. Te above shows
that the organisms produce ROS, if not adequately con-
trolled, through antioxidant systems; they are responsible
Hindawi
Evidence-Based Complementary and Alternative Medicine
Volume 2018, Article ID 9759240, 19 pages
https://doi.org/10.1155/2018/9759240