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Salvia officinalis is frequently used in traditional Algerian medicine to treat diverse microbial infections, including oral and vaginal candidiasis. The aerial parts of S. All the extracts were tested in vitro against several Candida species: C. Furthermore, the activity against biofilm-forming C. A large-scale extract was prepared via maceration in methanol, followed by fractionation on a silica gel column using increasingly polar mixtures of n -hexane, ethyl acetate, methanol, and acetic acid as mobile phase, to yield a total of fractions. Two major active fractions F and F , were further separated by HPLC, resulting in several active chromatographic peaks. Carnosol and methoxy-trans-carnosic acid were isolated as two major active compounds, and identified by a combination of NMR and mass spectrometry. The present study supports the traditional use of sage in the treatment of various fungal infections caused by Candida. Further studies of the bioactive compounds in an in vivo Candida biofilm model are required to validate their clinical potential as antifungals. Over the past decades, the incidence of fungal infections has dramatically increased, especially for systemic ones, due to a combination of reasons: the growing use of invasive medical devices e. Moreover, there is an increasing number of patients who survive with predisposing— e. These are able to cause infection that range from mild cutaneous—or mucosal—to severe systemic infections. Among Candida species, Candida albicans remains the most frequently isolated fungus from hospitalized patients Lohse et al. However, an increase in the proportion of infections caused by non- albicans Candida has been observed recently Pfaller et al. Despite advances in antifungal therapy, Candida infections continue to have a major impact on mortality and morbidity, as well as on the duration and cost of hospitalization Tanwar et al. This situation has led pharmaceutical companies and researchers to explore new alternatives, in order to discover improved antifungal agents that satisfy efficacy, safety, and economic criteria. Medicinal plants constitute one of these alternatives. Salvia officinalis L. Salvia sage is a perennial round shrub; its leaves and flowering tops are aromatic and used for the production of essential oils. Since antiquity this plant has been recognized for its medicinal importance Ghorbani and Esmaeilizadeh, It is used for the relief of pain, for protecting the body against oxidative stress, free radical damage, angiogenesis, inflammation, bacterial, and viral infections, as well as for a range of diseases including those of the nervous system, of heart and blood circulation, of the respiratory, digestive, metabolic, and endocrine system, etc. Istudor, ; Hamidpour et al. Algeria is one of the Maghreb countries where phytotherapy is frequently used by the population Allali et al. Based on recent publications of ethnopharmacology surveys in Algeria, we found that this plant is most commonly used, with use-values of 0. In fact, sage is used in the Ouargla province South-Eastern Algeria to treat foot ulcers, which are common there Telli et al. In the Msila region North Algeria , the infusion from its aerial parts is mainly used for diabetes, weight loss, as antihypertensive and for eczema Boudjelal et al. Similarly, people living in the region of Constantine and Mila North-East Algeria recommend it for the treatment of diverse diseases including nervous system diseases, muscle pain, headache, memory problems, as analgesic, as antispasmodic, for wounds, influenza, rheumatism, cholesterol lowering, gynecological diseases, and teeth problems Ouelbani et al. A decade ago, Horiuchi et al. Although Salvia is commonly used for several infections in Algeria, as well as in other parts of the world, the compounds responsible for its antifungal properties remain not well studied or fully explored. Therefore, the aim of the present study is to isolate the anti-Candida biofilm constituents from Salvia officinalis aerial parts through bioassay-guided purification. Lancashire, UK Panda et al. The flowering aerial parts of Salvia officinalis L. The plant material was identified by an experienced botanist Lakehal Samia using the descriptive reference of Quezel and Santa, The collected plant parts were dried for 1 week at ambient temperature to maintain their green color and volatile oils Panda, The dried raw botanical material was ground to a fine powder. Small-scale extractions were performed as described in our previous study Panda et al. In short, 1 gram of powder was transferred separately into each of four 15 mL sterile Falcon tubes, and extracted with four different solvents: acetone, hexane, methanol and water. Approximately g of the dried plant was weighed and transferred to a 2. The bottle was placed in a sonication water bath for four times 30 min every 6 h to maximize extraction. The extraction process was repeated until the yield became negligible. The dried residue of the methanol extract In each step of the gradient, 10 fractions of 40 mL each were collected in 50 mL conical Falcon tubes with screw caps. The following Candida strains were used for antifungal tests: C. A microdilution broth method was used as described previously by Panda et al. The percent inhibition of Candida strains was calculated according the following formula:. Where A is the OD value of a well with microbial culture and test sample, B the OD value of the corresponding negative control well with a mixture of pure broth and test sample and C the OD value of the average of two or more solvent control wells. The anti-biofilm activity of fractions and isolated compounds was determined by following the method described recently by Kipanga and Luyten on C. An overnight culture of C. The pellet was then washed with RPMI medium. Afterwards, each well was carefully washed using PBS without disturbing the biofilm layer at the bottom. A two—fold serial dilution up to 32—fold of a test compound was prepared in a 96—well conical-bottom V polystyrene microtitre plate. The BIC 50 for each growth condition was calculated by fitting the data to a non-linear least-squares sigmoid regression curve, fixing the top and bottom of the curve at and 0 percent, respectively. The chromatography data were acquired and processed using Lab Solution software. The mobile phase was composed of solvent A H 2 O with 0. A flow rate of 4. The active fractions were linked to the corresponding peaks by aligning the activity profile with the corresponding chromatogram Liu et al. Electrospray ionization ESI mass spectra were acquired in positive and negative ion mode. The results were recorded with the following ESI source parameters: end plate offset voltage of V, capillary voltage of 4, V, nebulizer of 2. The flow rate was 0. The mobile phase consisted of 0. For the initial testing, four different solvents viz. All these extracts were tested for antifungal activity in vitro against different Candida species Table 2. The methanol extract was most effective against both biofilm and liquid culture of C. Therefore, a large-scale methanol extract was prepared from g plant material, yielding This was separated on a silica gel column with a hexane-ethyl acetate-methanol-acetic acid step-gradient, resulting in fractions. Several of these Figure 3 were effective against C. Most of the activity was found in fractions between 26 and 45 with apparently two regions of maximum activity: F26 to 33 and F37 to 45 ; minor activity was centered around F72 and F Twenty fractions F26 to 45 were further tested by two-fold serial dilution to determine the most active fraction Figure 4. Fraction 31 and 39 were the most potent, and were further separated by HPLC. Table 2. Figure 2. Percent inhibition of C. Figure 3. Figure 4. Figure 5. Top HPLC chromatogram of fraction 31 F 31 of silica gel column see Figure 3 ; fractions were collected per minute and tested for activity percent inhibition of C. Figure 6. Top HPLC chromatogram of fraction 39 F 39 of silica gel column see Figure 3 ; fractions were collected per minute and tested for activity percent inhibition of C. The tentative identifications by mass spectrometry were confirmed by NMR. Table 3. Figure 7. Structures of carnosol A and methoxy-trans-carnosic acid B , isolated from the aerial parts of S. A non-linear regression of log inhibitor vs. The in vitro antimicrobial activity of Salvia officinalis was demonstrated decades ago Jalsenjak et al. Indeed, S. Essential oils of Salvia officinalis have been studied for activity against many Candida species C. Pinto et al. Also, Sookto et al. It appears that most previous studies on the antimicrobial and specifically the antifungal activity of S. Our study, on the other hand pertains to extracts containing primarily non-volatile components. Differences between the anti-Candida effects of Salvia officinalis extracts and essential oils may be due to the much higher concentration of compounds in, as well as different composition of the latter. For instance, the MIC of 1,8-cineole for C. Cardoso et al. Similar observations were also reported by Tan et al. Martins et al. It is not clear why alcoholic extracts were previously reported repeatedly to show no anti-Candida activity, whereas we could demonstrate it easily with methanol extracts. Perhaps it is due to differences in the location and time of collection of the botanical material, as well as post-harvest processing or extracting. In any case, our report seems to be the first to document anti-Candida activity in methanol extracts of S. Methanol is also believed to be a suitable solvent as it can efficiently penetrate cell membranes, permitting extraction of higher levels of endo-cellular components than solvents with lower polarity, and shows better antimicrobial properties Silva et al. Several studies on plant extracts from this species have focused on antimicrobial properties Bozin et al. Recently, Martins et al. The major compounds identified by LC-MS were derivatives of caffeic acid, rosmarinic acid, salvianolic acid, sagerinic acid, and luteolin, but the relationship between the presence of these compounds and the antifungal activity was not established Martins et al. Therefore, the compounds responsible for the antifungal activity of methanol extracts of S. Previous studies probably missed them because they are not major compounds identified in typical phytochemical studies. Carnosol was initially isolated from Salvia carnosa White and Jenkins, a , b and is presumably identical with a compound obtained from Salvia officinalis Janot et al. Horiuchi et al. Both carnosol and methoxy-trans-carnosic acid were reported as major components of Salvia fruticosa Exarchou et al. The compounds were also reported in S. This probably explains why they have not been identified so far as responsible for the antifungal activity of S. Abietane diterpenes like carnosic acid are a promising chemical class due to their abundance in medicinal plants and occurrence in industrial wastes San Feliciano et al. The compounds were demonstrated to have antioxidant Richheimer et al. Fischedick et al. From Salvia officinalis , these authors isolated carnosol, epirosmanol, rosmanol, carnosaldehyde, carnosic acid, methoxy-carnosic acid and sageone using different chromatographic techniques Fischedick et al. Dimayuga et al. Later, Dimayuga again studied the activity of carnosol in more pure form against the same strains, and concluded that the compound was active only against Gram-positive but not against Gram-negative bacteria, nor against the yeast C. They explained that the probable reason for their different results was the impure nature of the previous isolates, which had activity against many more test pathogens. The diterpene carnosic acid methyl ether methoxycarnosic acid was also isolated from S. These authors conclude that the antibacterial efficacy improved when carnosol was the major diterpene component. The antifungal activity of carnosol and methoxy-carnosic acid has so far been reported as weak. It is not clear why our findings are different, but the fact that some of the previously reported carnosol preparations were not pure, complicates the interpretation of their bioactivity. Further mechanism of action studies and molecular modeling need to be performed to identify the molecular targets of these compounds De Monte et al. Most researchers have found that carnosol has weak antimicrobial activity, but greatly reduced the MICs of various aminoglycosides and other types of antimicrobial agents Horiuchi et al. This may be due to efflux pump modulation by dissipation of the bacterial membrane potential Ojeda-Sana et al. It is not clear whether carnosol can also synergize with clinical antifungals. However, comparing our antifungal activity of the purified compounds with that of the total extract also suggests that the different isolated compounds probably act synergistically or at least additively. The widespread mode of microbial growth in most ecological niches is as biofilm, and C. Candida biofilms are intrinsically resistant to conventional antifungal therapeutics; as a result, biofilm-associated infections pose a major clinical challenge Gulati and Nobile, Previous studies on the anti-biofilm activities of Salvia species used its volatile oil. However, no study has thus far documented the antifungal biofilm properties of S. According to Hamidpour et al. In the Ames test on Salmonella it was found to have anti-mutagenic activity Minnunni et al. Not only in vitro , but several in vivo studies have suggested that daily oral administration of carnosol is well tolerated in animals. Ninomiya et al. Through bioassay-guided purification using the inhibitory activity against pancreatic lipase activity, four abietane-type diterpenes, including carnosic acid and carnosol, were isolated. Johnson and his co-workers Johnson et al. Recently, the European Union EU approved rosemary extracts, standardized to diterpenes e. All these data underscore the safety of oral carnosic acid and some of its analogs. A limitation of our study is that we have not exhaustively identified all antimicrobial components in the S. We have not pursued fractions with minor activity, and were unable to identify the bioactive compounds in some active chromatographic peaks due to the limited amount of material present. We found activity against non- albicans Candida species C. Further studies are needed to identify those compounds with antifungal activity against non- albicans Candida species. In summary, we isolated carnosol and methoxy-trans-carnosic acid from methanol extracts of Salvia officinalis and demonstrated that these are the two major compounds responsible for activity against C. Both compounds may have therapeutic potential by themselves or in combination with clinical antimicrobials. This will require more detailed evaluation in in vivo Candida biofilm models. All authors contributed to manuscript revision, read, and approved the submitted version. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. All other authors largely supported themselves. Abu-Darwish, M. Essential oil of common sage Salvia officinalis L. Allali, H. Phytotherapy of diabetes in West Algeria. Google Scholar. Aoyagi, Y. Cytotoxicity of abietane diterpenoids from Perovskia abrotanoides and of their semisynthetic analogues. Constituents of Salvia microphylla. Boudjelal, A. Herbalists and wild medicinal plants in M'Sila North Algeria : an ethnopharmacology survey. Bozin, B. Antimicrobial and antioxidant properties of rosemary and sage Rosmarinus officinalis L. Cardoso, A. Antifungal activity of plant based tinctures on Candida. De Monte, C. Bioactive compounds of Crocus sativus L. Enzyme Inhib. Anti-candida activity and cytotoxicity of a large library of new N-substituted-1, 3-thiazolidinone derivatives. Delamare, A. Antibacterial activity of the essential oils of Salvia officinalis L. Dimayuga, R. Traditional medicine of baja california sur Mexico. Edris, A. Chemical composition, antimicrobial activities and olfactive evaluation of a Salvia officinalis L. Essential Oil Res. Exarchou, V. Extract with antifungal potential: relevance of carnosic acid, carnosol and hispibulin. Fischedick, J. Structure activity relationship of phenolic diterpenes from Salvia officinalis as activators of the nuclear factor E2-related factor 2 pathway. Garber, G. An overview of fungal infections. Ghorbani, A. Pharmacological properties of Salvia officinalis and its components. Giannouli, A. The Genus Salvia , Vol. Kintzios Amsterdam: Harwood Academic Publication , 69— Gigante, B. Catechols from abietic acid: synthesis and evaluation as bioactive compounds. Gong, X. Invasive candidiasis in intensive care units in China: risk factors and prognoses of Candida albicans and non—albicans Candida infections. Synthetic derivatives of aromatic abietane diterpenoids and their biological activities. Gulati, M. Candida albicans biofilms: development, regulation, and molecular mechanisms. Hamidpour, M. Chemistry, pharmacology, and medicinal property of Sage Salvia to prevent and cure illnesses such as obesity, diabetes, depression, dementia, lupus, autism, heart disease, and cancer. Harriott, M. Importance of Candida-bacterial polymicrobial biofilms in disease. Horiuchi, K. Antimicrobial activity of oleanolic acid from Salvia officinalis and related compounds on vancomycin-resistant enterococci VRE. Potentiation of antimicrobial activity of aminoglycosides by carnosol from Salvia officinalis. Istudor, V. Bucuresti: Editura Medicala. Jalsenjak, V. Microcapsules of sage oil, essential oils content and antimicrobial activity. Pharmazie 42, — PubMed Abstract Google Scholar. Janot, M. Jasim, R. Inhibitory effect of aqueous Salvia officinalis leaves in the growth of Candida albicans from infected women with vaginal candidiasis. Al-Kindy College Med. Johnson, J. Carnosol: a promising anti-cancer and anti-inflammatory agent. Disruption of androgen and estrogen receptor activity in prostate cancer by a novel dietary diterpene carnosol: implications for chemoprevention. Relevance of carnosic acid, carnosol, and rosmarinic acid concentrations in the in vitro antioxidant and antimicrobial activities of Rosmarinus officinalis L. Khalil, R. Antimicrobial activity of essential oil of Salvia officinalis L. Kipanga, P. Influence of serum and polystyrene plate type on stability of Candida albicans biofilms. Methods , 8— Kojic, E. Candida infections of medical devices. Liu, M. Bioassay-guided isolation of active substances from Semen torreyae identifies two new anthelmintic compounds with novel mechanism of action. Lohse, M. Development and regulation of single- and multi-species Candida albicans biofilms. Manzoor, S. Laser induced breakdown spectroscopy for the discrimination of Candida strains. Talanta , — Martins, N. Evaluation of bioactive properties and phenolic compounds in different extracts prepared from Salvia officinalis L. Minnunni, M. Natural antioxidants as inhibitors of oxygen species induced mutagenicity. Nett, J. Fungal Biofilms: In vivo models for discovery of anti-biofilm drugs. Ninomiya, K. Carnosic acid, a new class of lipid absorption inhibitor from sage. Ojeda-Sana, A. Carnosic acid is an efflux pumps modulator by dissipation of the membrane potential in Enterococcus faecali s and Staphylococcus aureus. Oluwatuyi, M. Antibacterial and resistance modifying activity of Rosmarinus officinalis. Ouelbani, R. Ethno botanical investigations on plants used in folk medicine in the regions of Constantine and Mila North-East of Algeria. Panda, S. Ethno-medicinal uses and screening of plants for antibacterial activity from similipal biosphere reserve. Odisha, India. Assessing medicinal plants traditionally used in the Chirang Reserve Forest, Northeast, India for antimicrobial activity. Large scale screening of ethnomedicinal plants for identification of potential antibacterial compounds. Molecules 21, 1— Antimicrobial, anthelmintic, and antiviral activity of plants traditionally used for treating infectious disease in the similipal biosphere reserve, Odisha, India. Petiwala, S. Diterpenes from rosemary Rosmarinus officinalis : defining their potential for anticancer activity. Pfaller, M. Epidemiology and outcomes of invasive candidiasis due to non-albicans species of candida in 2, patients: data from the prospective antifungal therapy path registry — Pilmis, B. New clinical phenotypes of fungal infections in special hosts. Pinto, E. In vitro susceptibility of some species of yeasts and filamentous fungi to essential oils of Salvia officinalis. Quezel, P. Paris: CNRS. Quindos, G. Epidemiology of candidaemia and invasive candidiasis. A changing face. Razzaghi-Abyaneh, M. Antifungal Metabolites From Plants. Berlin; Heidelberg: Springer. Razzaghi-Abyaneh and M. Rai Berlin: Springer , 27— Richheimer, S. Antioxidant activity of lipid-soluble phenolic diterpenes from rosemary. Rus, C. Antifungal activity and chemical composition of Salvia officinalis L. San Feliciano, A. Abietane acids: Sources, biological activities, and therapeutic uses. Scheler, U. Elucidation of the biosynthesis of carnosic acid and its reconstitution in yeast. Silva, G. Investigation of effect of 1, 8-cineole on antimicrobial activity of chlorhexidine gluconate. Pharmacognosy Res. Singletary, K. Sookto, T. In vitro effects of Salvia officinalis L. Sur, S. Gas chromatographic determination of monoterpenes in essential oil medicinal plants. Tan, N. Antimycobacterial and antifungal activities of four selected Salvia species. Tanwar, J. Multidrug resistance: an emerging crisis. Telli, A. An ethnopharmacological survey of plants used in traditional diabetes treatment in south-eastern Algeria Ouargla province. Velickovic, D. Comparison of antioxidant and antimicrobial activities of extracts obtained from Salvia glutinosa L. Hemijska Industrija. Wang, L. Molecules 22, 1— White, A. Salvia curnoca U3ougl. I - A phytochemical study. Salvia carnosa U3ougl. II - Carnosol. Keywords: sage, carnosol, methoxy-trans-carnosic acid, biofilm, antifungal, Candida. The use, distribution or reproduction in other forums is permitted, provided the original author s and the copyright owner s are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher. Top bar navigation. About us About us. Sections Sections. About journal About journal. Article types Author guidelines Editor guidelines Publishing fees Submission checklist Contact editorial office. Introduction Over the past decades, the incidence of fungal infections has dramatically increased, especially for systemic ones, due to a combination of reasons: the growing use of invasive medical devices e. Figure 1. Map showing the zone of collection of Salvia officinalis. Table 1. Yield, color, and physical appearance of extracts. Edited by: Cassandra L.

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