Original ArticleBiomedicalEffect of Jujube Honey on Candida albicans Growth and Biofilm Formation
Introduction
Some Candida species are found as endosymbionts in most healthy individuals. C. albicans is the most common yeast found on the mucosal membranes of humans including in the oral cavity, esophagus, gastrointestinal tract, urinary bladder and genitalia (1). In immunocompromised individuals, C. albicans has emerged as a true opportunistic pathogen. This yeast adheres to and colonizes epithelial tissues and causes superficial and life-threatening infections. C. albicans has become one of the main causes of morbidity and mortality worldwide among immunocompromised individuals (2). Importantly, Candida has been shown to be the third most commonly isolated blood pathogen from patients in U.S. hospitals (3).
According to the National Institutes of Health (USA), more than 60% of all microbial infections are associated with biofilms (4). Biofilms are particularly problematic in the clinical environment and, like bacteria, various fungal species can form biofilms in vivo and in vitro (5). Among fungi, C. albicans is the most common pathogen associated with fungal biofilm infections, especially infections related to implanted medical devices (6). A common issue associated with C. albicans biofilms is the increased resistance of these biofilms to antifungal agents such as azole drugs and their derivatives and to host immune defenses. The increased resistance is due to the extracellular matrix secreted by the Candida cells, which shields the Candida cells from antibodies and prevents drugs from penetrating the biofilm 7, 8. The emergence of resistant C. albicans has a major impact on public health and the economy. Because of the increasing prevalence of drug-resistant C. albicans, there is an urgent need to develop alternative treatments for Candida infections that are safe, effective and inexpensive.
Among all of the strategies that have been exploited to overcome drug resistance, the use of natural substances has shown particular promise, and many natural substances have been found to have antifungal properties (9). Bee products such as honey and propolis are rich sources of essential bioactive compounds. Because of its medicinal qualities, honey has been used for the management of many diseases throughout the ages and has become a traditional remedy for treating microbial infections and wounds 10, 11, 12, 13, 14. The Talmud, the Old and New Testaments of the Bible, and the Holy Qur'an (1400 years ago) mentioned honey as a cure for diseases. A large chapter (SORA) presents in the Holey Qur'an named BEE (Al Nahl) and part of it says (And thy Holy LORD taught the bee to build its cells in hills, on trees and in men's habitations, then to eat of all the produce of the earth and find with skill the spacious paths of its LORD, there issues from within their bodies a drink of varying colors, wherein is healing for men, verily in this is a sign for those who give thought).
The antimicrobial properties of honey depend on its type, flower source, botanical and geographical origins and the harvesting, processing and storage conditions used 12, 15, 16. Honey is widely used in the Arabian peninsula for nutritional and therapeutic purposes; however, no research has been conducted on the antimicrobial activity of regional honey collected in the Arabian peninsula. The antimicrobial effects of honey on Staphylococcus aureus, Pseudomonas aeruginosa and other bacterial biofilms have been studied 17, 18, 19, 20. Honey also reduces the production of an extracellular polysaccharide matrix while promoting the disruption of mature biofilms 21, 22. The effect of honey on C. albicans biofilms has not been extensively studied 23, 24, 25, 26, 27, 28, 29. To our knowledge, no research has been conducted on the effect of honey on C. albicans biofilms. A better understanding of C. albicans responses to honey may facilitate its use as a biofilm inhibitor. The aim of this study was to use broth dilution assay followed by the determination of the minimum inhibitory concentration (MIC) of jujube honey and use of new techniques like scanning electron microscopy (SEM), atomic force microscopy (AFM) and Fourier transform infrared (FTIR) spectroscopy to investigate the in vitro effects of jujube honey on planktonic states of C. albicans and detachment of biofilm-embedded states.
Section snippets
Honey
Natural jujube honey was used throughout this study. This honey was obtained from the beekeepers' association of Al-Baha, Saudi Arabia in a 1-kg sterile container. The honey was obtained directly from the honeycomb by pressing and was filtered to remove the wax and other impurities. This natural honey was passed through 45-μm-pore-size filters and stored at −4°C until use.
Microorganisms and Culture Conditions
The test organism used in this study, C. albicans ATCC 10231, was provided by the College of Medicine, King Saud University
Determination of the Minimum Inhibitory Concentration
Jujube honey inhibited C. albicans ATCC 10231 growth in a concentration-dependent manner. The MIC of jujube honey against biofilm-forming C. albicans ATCC 10231 was 40% (w/v), and the minimal fungicidal concentration (MFC) was 50% (w/v). The MFC is defined as the lowest concentration of honey resulting in the death of 99.9% of the inoculum. In general, the MFC value is greater than the MIC value. The growth curves of yeast exposed to 40% (w/v) jujube honey showed a reduced growth rate and a
Discussion
Honey is widely used in a variety of household recipes. Honey is an excellent natural food product rich in minerals, antioxidants and simple sugars. Honey can prevent deteriorative oxidation reactions in foods such as the browning of fruits and vegetables and lipid oxidation in meat. Honey inhibits growth of foodborne pathogens and microorganisms that cause food spoilage 33, 34.
Several studies conducted on the antimicrobial properties of honey have confirmed that honey is effective at treating
Acknowledgments
The authors are thankful to National Plan for Science and Technology (NPST) program by King Saud University Riyadh, Project No. 11-AGR1748-02 for financial support.
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