Journal of Food Quality

Journal of Food Quality / 2019 / Article

Research Article | Open Access

Volume 2019 |Article ID 3707219 |

Rajaa Seghiri, Mourad Kharbach, Azzouz Essamri, "Functional Composition, Nutritional Properties, and Biological Activities of Moroccan Spirulina Microalga", Journal of Food Quality, vol. 2019, Article ID 3707219, 11 pages, 2019.

Functional Composition, Nutritional Properties, and Biological Activities of Moroccan Spirulina Microalga

Academic Editor: Francisca Hernández
Received25 Jan 2019
Revised28 Apr 2019
Accepted20 May 2019
Published03 Jul 2019


The present study aimed to characterize the nutraceutical properties and the antimicrobial effect of Moroccan Spirulina (Arthrospira platensis). The nutritional composition was evaluated, including water content, crude protein, total carbohydrates, lipids, phenolic composition, macro- and micromineral content, fiber content, and energy value. Then, the microbiological analysis and antioxidant activity were measured. The antimicrobial activity was evaluated using the minimum inhibitory concentration method on bacteria and fungi. Moroccan Spirulina contained a large amount of protein (76.65 ± 0.15%), followed by carbohydrates (6.46 ± 0.32%), minerals (20.91 ± 0.88%), crude fiber (4.07 ± 1.42%), lipids (2.45 ± 0.82%), ash (14.56 ± 0.74), and twenty phenolic acids being identified and quantified. Moreover, flavonoid and phenolic contents were present at 15.60 ± 2.74 mg RE/g dw and 4.19 ± 0.21 mg GAE/g dw, respectively. Microbiological risk assessment indicated that this product is safe to be consumed as a human food product. The antioxidant activity was higher in the methanolic fraction (23 mg TE/g dw) (DPPH).

1. Introduction

The Moroccan coast extends over 3500 km (2900 km for the Atlantic coast and 500 km for the Mediterranean coast). This ecosystem was recognized as vital and fragile but with a considerable ecological value. Despite increasing recognition of different foods and their safety, algae have received small interest in spite of their wide and abundant availability. Algae were one of the first life forms on Earth, and several thousand species existed [1]. On the contrary, microalgae were considered an important part of aquatic biodiversity; they were grown in different environments (sea, freshwater, and desert) and also in different forms (single cells, colonies, or filaments) [2]. Recently, algae have been used as food supplements in order to enhance their nutritional value, as animal feed additives, and even for pharmaceutical uses [3, 4]. However, they have diverse chemical properties and were marketed in various forms, mainly powder, tablets, straw, capsules, and liquids, or incorporated to other foods, such as pasta, gums, and beverages [5]. On the contrary, microalgae are an alternative food of natural antioxidants, which were more varied than those found in other terrestrial plants [6]. Polyphenolic compounds were known as important natural antioxidants, while numerous classes of flavonoids and other classes of phenolics were found in microalgae. In addition, various polyphenolic molecules were associated with biopharmacological activities including antimicrobial and antioxidant actions [7, 8]. The commercial strains of edible microalgae were mainly dominated by Chlorella, Arthrospira, Dunaliella salina, and Aphanizomenon flos-aquae. Towards a more food-secure future, the Spirulina cyanobacterium (Arthrospira platensis) became trendy health food brands, which explained its culture in several countries [9]. Various companies sell a variety of Arthrospira-based products (tablets and powder) as a food supplement and distribute them to over 20 countries around the world. Therefore, they have been widely introduced (fresh or dried) in the human diet and nutrition.

Spirulina is an abundant source of nutritious composition, including protein, vitamins, lipids, fibers, minerals, carbohydrates, and some of natural pigments [10]. Spirulina was recognized as a safe supplement (GRAS) without toxicological effect and was officially approved by the Food and Drug Administration (FDA) and the National Sanitary Surveillance Agency (ANVISA). These main constituents confer a physiological potential and a functional benefit that makes it promising for the food industry to overcome the problem of malnutrition and in health applications against pathogens [11, 12]. Right from the beginning of the applied phycology, the algae’s chemical composition and their main bioactive compounds have received an intense interest [13]. The nutritional and toxicological assessments of commercial algae foodstuff were little studied and often based on reports from field or interlaboratory ecological or physiological studies [14]. According to the best of our knowledge, no studies have been performed on the nutraceutical properties of a strain of Spirulina isolated in Morocco. The present work aims to evaluate the Moroccan Spirulina’s nutritional and pharmacological properties. Firstly, the chemical and nutritional compositions including phenolic profiling were investigated. Secondly, antimicrobial and antioxidant activities were evaluated.

2. Materials and Methods

2.1. Raw Materials

Spirulina platensis (Arthrospira platensis) used in this study was provided by the Spirulina-Berbère® company, located in the region of Souss-Massa-Drâa, in the south of Morocco. From an artificial pond culture in March 2016, the microalga was grown by company’s process on Zarrouk’s medium implemented under cover in a greenhouse under the following environmental conditions: at pH = 10.25, salinity = 16, and shading = 65% and under the solar light between 23 and 30°C with constant shaking. Growth was monitored by measuring water transparency using the test of Secchi. After harvesting and spinning, microalga cake was dried in a hot air oven at 70°C. Finally, dried samples were crushed and sieved at 1 mm pore diameter to obtain a fine and homogeneous powder using a mill (MF 10 basic, IKA-WERKE). The powder was stored in sealed plastic bags in desiccators at room temperature for further chemical analysis. To facilitate reading, Spirulina was used as a generic name for commercial products from Arthrospira spp.

2.2. Chemicals and Reagents

All chemical reagents and solvents used were provided by Sigma-Aldrich (St. Louis, MO). Bacterial strains studied are in the form of batches by the American Type Culture Collection (ATCC), maintained by subculture on nutrient agar favorable to their growth, and obtained from the Fungus Collection Mycology Laboratory of the Forest Research Centre of Rabat, Morocco.

2.3. Nutritional Value

Protein, carbohydrates, lipids, fibers, ash, and micronutrient content were expressed on a microalga dry weight basis, and the results were presented in g/100 g. Analyses were carried out in three replicates.Ash content: it was determined by AACC [15]. Samples were preweighed in a crucible and combusted in a muffle furnace (Nabertherm, 30–3000°C) at 550°C for 4 hours. Then, they were cooled with the door left open and weighed, and the ash content was calculated.Moisture: it was measured by drying at 80°C for 24 h, and the samples and their results were reported on a dry weight basis [16].Crude protein (CP): it was quantified using the Kjeldahl method by the AOAC [17].Crude fat (fat): it was determined using the Soxhlet method by the AACC [15]. It was extracted with ethyl ether, and the obtained mixture was concentrated under vacuum. The obtained fat was weighed and expressed as a percentage (%).Total fiber fractions: crude fiber (CF) was assessed according to the AOAC method [17]. The neutral detergent fiber (NDF), acid detergent fiber (ADF), and acid detergent lignin (ADL) were determined according to the method described in [18]. In fact, for each sample, all fiber fractions previously mentioned were sequentially determined. The obtained hemicellulose was calculated according to the method in [19].Mineral composition: macroelements including K+ and Na+ contents were determined using a flame photometer, while Mg2+ and Ca2+ contents were determined using complexometric titration. On the contrary, phosphorus content was measured by using the acidified solution reaction of ammonium molybdate containing ascorbic acid and antimony [20]. Microelements including Cu, Zn, Fe, Mn, and Ni were determined using atomic absorption spectrometry in the air-acetylene flame [21].Carbohydrates (CHO): they were quantified according to the method in [22], by a difference of all other components as weight in grams minus water, fiber, ash, fat, and protein content.Energy value (E): it was calculated according to the method in [22], by calculating the approximate composition data. Energy (kcal) was calculated according to the following equation:

Values were expressed in kcal/100 g.

2.4. Microbiological Quality

The microbiological stability of the packaged sample was analyzed by measurement of total aerobic mesophilic flora (NF EN ISO 4833), Staphylococcus (NF EN ISO 6888-2 at 37°C), total coliforms (NFV 08-050 at 30°C), fecal coliforms (NFV 08-060 at 44°C), sulfite-reducing Clostridium bacteria (NFV 08-061), yeasts and molds (NF V08-059 at 28°C), Salmonella (NF EN ISO 6579), and enterobacteria (NF V 08-054).

2.5. Physicochemical Analysis and Characterization
2.5.1. Total Polyphenol Assay

It was estimated by the Folin–Ciocalteu method [23]. Gallic acid was used as a standard curve for quantification of PC. The results were expressed as gallic acid equivalent (GAE)/g of dry matter of Spirulina.

2.5.2. Total Flavonoid Assay

It was assessed by applying the aluminum chloride colorimetric method according to the study in [24]. Flavonoid concentrations were deduced from the range of the calibration curve established with quercetin. The results were expressed in milligram equivalents of quercetin per gram of dry matter (mg EQ/g dry matter).

HPLC-DAD-QTOF/MS Analysis of Polyphenolic Composition. The Agilent 1100 high-performance liquid chromatography (HPLC) system (Agilent Technologies, Inc., Wilmington, DE, USA) is composed of a diode array detector (DAD) (G1315B), an autosampler (G1330B), and a binary pump (G1312A). The mass spectrometer (MS) detector was connected to an electrospray ionizer (Micromass Quattro Micro; Waters Technologies, Milford, MA, USA). The elution separation was carried out in a reverse phase based on Zorbax column phase C18 (Agilent Technologies; 100 mm × 2.1 mm × 1.7 μm). The following chromatographic conditions were applied: injection volume 10 μl; column temperature 35°C; flow of injection 0.5 ml/min; mobile phase compositions: acetonitrile with 0.1% formic acid (A) and 0.1% formic acid in water (v/v) (B); and gradient elution (v/v): 10% A (0 min), 70% A (18 min), 10% A (2 min), 10% A (3 min), 10% A (2 min), and 10% A (5 min). The negative mode was applied with the following conditions: voltage of capillary 3.0 kV, voltage of cone 20 V, voltage of extractor 2 V, temperature source 100°C, desolvation temperature 350°C, desolvation gas flow 350 l/h, and cone gas flow 30 l/h. The phenolic acid peak identification was carried out by comparison of retention times and MS spectra with those of pure standards and by molecular ion identification (Sigma-Aldrich, France). On the contrary, the quantification of phenolic acids was done based on standard calibration curves. Spirulina samples were ground as powder, dissolved in water in order to obtain 1 mg/mL concentration, and then filtered by a 0.2 μm (PVDF) syringe filter prior to the chromatographic analysis.

2.6. Bioactivity Analysis
2.6.1. Preparation of Methanolic Extract

10 g of each powder sample was crushed in a solvent (MeOH) (1 L) for 48 h at 24°C in dark and stirred [25] with slight modifications. The extracts were centrifuged at 5000 rpm for 15 min, filtered, diluted with 10% of dimethyl sulfoxide (DMSO), and then stored in glass vials in dark at 4°C before use. DMSO was used as a negative control.

2.6.2. Antioxidant Activity

The radical-scavenging 2,2-diphenyl-1-picrylhydrazyl (DPPH) test was used. Each test was repeated in triplicate. The procedure was followed as described by Lopes-Lutz [26].The DPPH solution (5.91 mg of DPPH and 50 ml of methanol) was mixed with methanolic extracts at a different concentration (2–600 μg/ml) (1 ml; 0.3 mM) of DPPH and then incubated for 30 min in dark. A solution control (blank) was prepared by dissolving the DPPH solution in pure methanol. The reduction in DPPH free radicals was determined at 517 nm. The positive control was prepared with L-ascorbic acid, and the inhibition ratio (%) was calculated using the following equation:

The antioxidant activity of each sample was determined based on the inhibition curve and was expressed in terms of IC50.

2.6.3. Antimicrobial Assays

The minimum inhibitory concentrations (MICs) of the methanolic extract were assayed according to the procedure described in [27] and modified in [28, 29]. In vitro antibacterial studies were carried out against four bacterial strains: the Gram-positive bacteria S. aureus, B. subtilis, and M. luteus and the Gram-negative bacterium E. coli. Moreover, one mold (Aspergillus niger) and one mushroom wood rot (Coriolus versicolor) were also employed. Quantities of these extracts were added to test tubes containing nutrient agar at 0.2% for bacteria and potato dextrose agar (PDA) for molds to promote germ/compound contact in test tubes. Each contained 13.5 ml tryptic soy agar medium, sterilized by autoclaving (20 min at 121°C), cooled to 45°C, and then poured into Petri dishes. 1.5 ml of each dilution was added in such a way to obtain a final concentration of 1/100 to 1/5000 (v/v). Controls consisting of the medium plus 0.2% agar-agar solution alone were also prepared. The results were considered in the context of calibrated platinum loops in the same volume of inoculum. The inoculum was in the form of culture broth (24 h, 37°C) for bacteria and in the form of suspension in physiological water of spores from a seven-day culture (7 d, 25°C) in the PDA for molds. Each test was done in triplicate to minimize experimental error.

2.7. Statistical Analyses

Results were expressed as mean values ± standard deviation of three separate determinations.

3. Results and Discussion

3.1. Gross Biochemical Composition

Microalgae were considered an alternative source of protein, thanks to their high content of proteins [30]. The gross chemical composition of the analyzed Spirulina is summarized in Table 1.

ElementsPercentage (%)bOther micro/macroalgae

Moisturea (%)12.66 ± 1.7<9% [48]
Ash (%)14.56 ± 0.747.4–10.4% [5, 37, 54]
4–20% [55, 56]
Protein (%)76.65 ± 0.1560–71 [5, 36, 37],
6–71% [3945]
3–47% [46, 47]
Lipids (%)2.45 ± 0.826–13% [5, 37]
>60% [3945]
>5% [46, 47]
CF (%)4.07 ± 1.421.36–7.73% [53]
Carbohydrates (%)c6.46 ± 0.3215–25% [5, 36, 37]
10–27% [3945]
20–68% [46, 47]
Energy (kcal/100 g)436.18 ± 2.29ND

Note.aExpressed as percentage of freeze-dried samples. bData are mean values ± SD of three determinations. cCalculated by difference (=100  crude protein  crude lipid  total dietary fiber (TDF)ash). Dried Spirulina sp. % at 70°C of cell constituents is calculated after the moisture content was subtracted. ND: not detected.

The Moroccan strain studied contains a considerable amount of protein (76.65 ± 0.15%). This value was higher than that of various Spirulina species harvested from other countries [31, 32], with its amino acid composition of aspartic acid, glutamic acid, serine, glycine, histidine, arginine, threonine, alanine, proline, valine, isoleucine, leucine, phenylalanine, and lysine shown in [33]. It also showed a fairly high protein concentration compared to some of other microalgae (6 to 71%) [34, 35]. It was also higher than that of the most of red and green seaweeds (10 to 47%) of dry matter [36] and brown edible seaweeds (3 to 15% dw) [37]. This result confirms that the protein content in Spirulina was considerably higher than those in some plants [5]. Furthermore, several studies have demonstrated that the protein content of microalgae varied according to species, environmental conditions, and analytical methods for protein determination [38, 39].

Lipids represent one of the main sources of energy for human metabolic processes. Spirulina lipid contains polyunsaturated fatty acids (PUFAs), mainly γ-linoleic acid with 30 to 35% of total lipid content, which are functional and structural components of cell membranes, while the main lipid membrane constituents in Spirulina are glycolipids and the essential fatty acids from the ω3 and ω6 families [40]. The Moroccan samples contained 2.45 ± 0.82% dw of fat. This value was much lower than that reported in previous studies on other Spirulina products (6 to 13%) [31, 32]. On the contrary, it was lower than the content of marine and some freshwater microalga species where lipid content was above 60% of dw [34, 35]. Although it was reported that edible lipid seaweed content does not obviously exceed 5% of dry matter, our result is also following the literature range [36, 37]. This result confirms that Spirulina appears very favorable for low-fat diets relatively to vegetables [5, 42]. Furthermore, this difference might relate to the strain, different extraction methods, solvents used, or nutritional and environmental factors [50].

Microalga carbohydrates (e.g., starch, glucose, sugars, and other polysaccharides) normally generate energy and cellular structure. The carbohydrate content was about 6.46 ± 0.32%. This value was considerably lower than the carbohydrate concentration average of 15 to 25% reported previously for other Spirulina strains [31, 32]. Besides, the Spirulina studied showed a carbohydrate content typically below average for many microalgae, overall accounting for 10 to 27% dw [34, 35]. In addition, it was lower than that reported in edible seaweeds which ranged from 20 to 68% [36, 37, 43]. The soluble carbohydrates constitute a major part of the total carbohydrate content, whereas in higher plants, insoluble carbohydrates are a major constituent of total carbohydrates [44]. This result agrees with other reports that showed dried whole microalgae can be used as food due to their higher carbohydrate digestibility. However, like carbohydrate composition, the protein content of algae was linked to the seasonal variation [50].

Algae were characterized by a higher ash content. The ash content for Moroccan samples was 14.56 ± 0.74%. This value was higher than that found previously in other Spirulina species (7.4 to 10.4%) [31, 32, 45]. This value might be high because of inadequate grinding of the samples prior to analysis. Indeed, ash content of our Spirulina was found as 20% which was also compared with freshwater and marine microalgae which range from 4% to 20% [46]. However, it was lower than the ash content shown in edible seaweeds, which in general have a high content of minerals reflected in the ash content [36, 37, 47].

Moisture is an important factor for assessing the microalga quality. The dry matter content was 87.70 ± 1.85%. In fact, companies provide standards in their nutritional information and set the moisture standard below 9% [48]. This value could be due to drying methods and drying time [49]. On the contrary, the packaging and the storage conditions might have an indirect influence on the humidity rate. The microalgae should not be dried extremely because it could change the structure of living cells which would degrade their physicochemical properties. Therefore, their overall quality will not be optimal.

The dietary fiber content of algae was of high nutritional importance. The present study was focused on the determination of crude fiber (CF, lignocellulose complex) and some polysaccharides of fibrous nature which would be identified further by future studies using highly sophisticated techniques. The cellulose and hemicellulose play an important role as structural components of the cell wall in algae [50]. The crude fiber content was 4.07 ± 1.42% higher than that from seaweeds [51] and than that from terrestrial plants or vegetables [52]. Besides, the value was in the middle of the seaweed content (1.36–7.73%) [53]. Therefore, Moroccan Spirulina might be considered as a good source of dietary fiber like several edible seaweeds.

Generally, algae were considered to have a high ash content, essential minerals, and trace elements required for human nutrition. Given the ash content in Spirulina in Table 1, a high mineral content was predicted. Nutrient sufficiency is essential for productivity and longevity. The mineral result analyses are shown in Table 2. The studied microalga contained higher amounts of the macrominerals (32694.32 ± 6175.08 mg/100 g·dw) and trace elements (88.44 ± 3.2 mg/100 g·dw) required for human nutrition [54]. In addition, it contained significant amounts of essential minerals such as P (10088.33 ± 5766.88), Na (14004 ± 397.55), K (2501.66 ± 4.22), Ca (6000 ± 4.66), and Mg (100.33 ± 1.77 mg/100 g·dw), respectively. Trace elements were also detected (Fe, 80.66 ± 1.77; Zn, 5 ± 0.66; Cu, 1.22 ± 0.66; and Mn, 1.56 ± 0.11 mg/100g·dw, respectively). The macroelements found were slightly higher than those found in marine microalgae, which is interesting as Zarrouk’s medium supplies them in excess, except for Mg which displays a lower value compared to them. Otherwise, the microelements Cu, Mn, and Fe were presented in the microalga studied with modest values compared to marine microalgae, excluding the Zn content [55]. These results were relatively higher than those of the most land plants (5–10%) [56]. The mineral content is highly related to physiological and environmental factors, processing, and mineralization methods involving dry mineralization in an oven at 550°C [17, 57]. Consequently, the study confirms that Spirulina’s benefits may be attributed to both mineral and trace element contents.

ElementsSpirulina studiedOther microalgae [55]

Minerals (mg/100 g dw)P10088.33 ± 5766.881700–3000
Na14004 ± 397.557000–1100
K2501.66 ± 4.22600–1200
Ca6000 ± 4.66300–2100
Mg100.33 ± 1.77100–1100

Trace elements (mg/100 g dw)Fe80.66 ± 1.77100–700
Zn5 ± 0.6623.9–370
Cu1.22 ± 0.661.2–65
Mn1.56 ± 0.113.7–59.2

3.2. Microbiological Analysis

The edible product was exposed to all contamination vectors. The microbial monitoring of marketed Spirulina powder is necessary since it is possible to affect the product quality by reducing the availability of nutrients. The microbiological quality of edible Spirulina is shown in Table 3. With respect to pathogenic microorganisms, the presence of total coliforms and Staphylococcus (<100 cfu/100 ml) may present a hazard. However, the absence of fecal coliforms indicates hygienic standards of the adopted technology and preparation were respected. Salmonella and sulfito-reducer bacteria, specifically Clostridium perfringens, were also not detected. The presence of enterobacteria, in particular Escherichia coli at 40%, which should be absent according to the EU standard, indicates fecal contamination. Finally, the yeasts and molds present in the ground and feces may have been transmitted via dust by wind, insects, or equipment. In fact, the microbial qualities of the samples from the routinely cultivated biomass by the company were moderately satisfactory according to the European Union and World Health Organization standards. In order to ensure its safety as food, it was necessary to control total coliforms, Staphylococcus, and Escherichia coli which could be responsible for toxicity potential. Otherwise, except the negative findings, these results were in agreement with those shown in [58], which confirmed that the microflora associated with Spirulina crops was generally nonpathogenic. In addition, a high alkalinity of the Spirulina environment is normally an excellent barrier to contamination, whether by bacteria, fungi, or algae. Furthermore, certain substances of both intracellular and extracellular metabolites as antimicrobial agents such as terpenols, sterols, polysaccharides, dibutenolides, peptides, and protein metabolites secreted by or present in Spirulina have a bactericidal or at least bacteriostatic effect on humans [59, 60]. The final microbial load of the product has been reported to depend on how carefully the culture and product are handled at various stages [61]. Therefore, subsequent handling of the product during harvest, drying, and packaging is very important and in this case appears to be generally satisfactory (Figure 1).

PathogensAll aerobic mesophilic floraStaphylococcusTotal coliformsFecal coliformsSulfito-reducer bacteriaYeasts and moldsE. coliSalmonella

Bacterial count2089326NDND144.15ND
EU standard105AbsentAbsentNo data104104AbsentAbsent
WHONo dataNo dataNo dataNo data103No dataAbsent

EU, European Union [41]; WHO, World Health Organization [42]; ND: not detected.
3.3. Phytochemical Analysis and Characterization
3.3.1. Total Phenolic Content (TPC) and Total Flavonoid Content (TFC)

Spirulina was considered a good source of nutritional phenolic and flavonoid compounds due to its higher production capacity compared to conventional plant-derived sources. As shown in Figure 2, the TPC and TFC of methanolic extracts from Spirulina were determined in terms of milligrams of gallic acid equivalents per gram of dry weight (mg GAE/g dw) from the calibration curve of gallic acid and milligrams of quercetin equivalents per gram of dry microalga extract (mg QE/g DE) through the calibration curve of quercetin, respectively. The obtained results revealed the presence of polyphenols (0.287 mg GAE/g DW) and total flavonoids (0.166 mg QE/g DE). These results were in agreement with the total phenolic content level (<5 mg GAE/g DW) for different microalgal species and also for different extracts [62, 63]. Phenolic compounds are secondary metabolites commonly found in Spirulina [64], with some of the main forms being salicylic, chlorogenic, synaptic caffeic, and trans-cinnamic acids, which have been known for their chemical protective mechanisms against some agents of biotic and abiotic stresses [65]. It also contains various classes of flavonoids like isoflavones, flavonols, flavanones, and dihydrochalcones. These natural phenolics have probably a broad spectrum of chemical and biological properties including antioxidant and free radical-scavenging activities. Moreover, the total phenolic contents obtained showed significant variations [66] which could be explained by geographical, physiological, and environmental factors and culture conditions [67].

3.3.2. Phenolic Acid and Flavonoid Composition

A chromatographic separation method (HPLC-DAD/MS) was developed for simultaneous identification and quantification of phenolic acids and flavonoids in Spirulina reported to possess vital nutritional and biological activities [68]. A total of twenty phenolic acid and flavonoid compounds were properly identified and quantified compared with phenolic standards (retention times, mass spectra, and their fragmentations) within 30 min. Table 3 shows the quantification results and some information about phenolic acids and flavonoids (molecular formula, molecular weight, [M-H] values, mass spectra, and retention times) in an aqueous extract from Spirulina. The phenolic and flavonoid amounts in an aqueous extract were determined, and the extract was rich in succinic acid (1122.88 mg/kg), followed by quinic acid (844.17 mg/kg), 3-4-hydroxybenzoic acid (687.07 mg/kg), catechin (584.53 mg/kg), citric acid (64.06 mg/kg), vanillic acid (16.24 mg/kg), gallic acid (2.13 mg/kg), 4-hydroxybenzoic acid (1.07 mg/kg), and trace elements (<1 mg/kg) of rutin, chlorogenic acid, quercetin, rosmarinic acid, salicylic acid, resveratrol, pyrogallol, ferulic acid, 4-hydroxycinnamic acid, 3-hydroxycinnamic acid, and 2-hydroxycinnamic acid. A list of other phenolic acids and flavonoids is also shown in Table 4. The phenolic acid amounts were varied in Spirulina species depending on culturing conditions [67, 69]. Only gallic, caffeic, salicylic, chlorogenic, and trans-cinnamic acids were detected in previous studies with Spirulina algae [69, 70].

Phenolic acidsSpirulinaMolecular formulaMolecular weight (M)HPLC-ESI/MS (m/z)
RT (min)[M-H]

Quinic acid844.17 ± 42.21C7H12O6192.1670.51191.120
Citric acid64.06 ± 3.20C6H8O7192.1230.63191.102
Pyrogallol0.42 ± 0.02C6H6O3126.1110.64125.024
Succinic acid1122.88 ± 56.14C4H6O4118.0880.65117.018
Gallic acid2.13 ± 0.11C7H6O5170.0220.66168.90
Chlorogenic acid0.86 ± 0.04C16H18O9354.3110.83353.202
3,4-Hydroxybenzoic acid687.07 ± 34.35C7H6O4154.1210.95153.010
4-Hydroxybenzoic acid1.07 ± 0.05C7H6O3138.1221.30137.050
Catechin584.53 ± 29.22C15H14O6290.2711.63289.064
Vanillic acid16.24 ± 0.81C8H8O4168.1482.12167.036
4-Hydroxycinnamic acid0.12 ± 0.01C9H8O3164.1602.21163.042
Rutin0.93 ± 0.05C27H30O16610.1532.63609.1
3-Hydroxycinnamic acid0.15 ± 0.01C9H8O3164.1602.98163.042
Ferulic acid0.48 ± 0.02C10H10O4194.1863.12193.050
Quercetin0.01 ± 0.00C15H10O7302.2383.48301.000
2-Hydroxycinnamic acid0.31 ± 0.02C9H8O3164.1603.65163.042
Salicylic acid0.08 ± 0.003C7H6O3138.1223.68137.025
Rosmarinic acid0.18 ± 0.01C18H16O8360.3184.01359.054
Resveratrol0.10 ± 0.005C14H12O3228.2475.83227.072
Quercitrin0.04 ± 0.00C21H20O11448.385.99447.120
Epigallocatechin gallateNDC22H18O11458.375ND457.078
Malic acidNDC4H6O5134.087ND133.014
Syringic acidNDC9H10O5198.174ND197.045
3-Hydroxybenzoic acidNDC7H6O3138.122ND137.025
Benzoic acidNDC7H6O2122.123ND121.031
Caffeic acidNDC9H8O4180.159ND179.035
Sinapic acidNDC11H12O5224.212ND223.061
Tannic acidNDC76H52O461701.206ND1700.080

ND: not detected.
3.3.3. Antioxidant Bioactivity Analysis

The total antioxidant capacity (TAC) of the methanolic extract was determined using the DPPH radical-scavenging assay. The results are displayed in Figure 3.

The DPPH radical-scavenging activity was generally quantified in terms of inhibition percentage of the preformed free radical by antioxidants and EC50 (concentration required to obtain a 50% antioxidant effect) [71]. The EC50 was widely used to express the antioxidant capacity and to compare the activity of different compounds. In this study, the EC50 was 23 μg/ml, indicating a very high antioxidant potential [72]. Both the lower EC50 and the higher DPPH activity were related to a high antioxidant activity [73]. The study has been carried out on the DPPH-scavenging activity of the Spirulina extract compared to both vitamins C and E which showed that EC50 was about 40 ppm; i.e., one is better than the other which is comparable, as shown in [71]. Previous reports have revealed that the antioxidant activity of Spirulina may arise from a whole spectrum of natural antioxidant compounds that contribute to the oxidation process inhibition [74]. The phenolic compounds are mostly found in extracts of higher polarity and seem to be related to antioxidant activity or synergistic action, thanks to their redox properties [75]. However, the presence of different antioxidant compounds in the methanol extract was responsible for the free radical-scavenging activity, either individually or synergistically.

3.3.4. Antimicrobial Activity

The growth of pathogenic and contaminant microorganisms in food decreases the nutritional quality and increases food toxicity. The antimicrobial activity of the methanolic extract of Spirulina against microorganisms that contaminate food products was investigated. The results are presented in Table 5. The methanolic extract had no antimicrobial activity against the bacteria and molds studied. Nevertheless, it had antifungal activity against Coriolus versicolor, with a minimum inhibitory concentration (MIC) between 1/250 and 1/100 v/v of 1 g/10 ml. These results disagree with those of previous studies, in which Spirulina has been declared as bioactive-rich compounds in that microbial growth could be promoted or inhibited [76]. Indeed, it has been reported that the methanolic extract of Spirulina platensis possesses antimicrobial and antifungal potential against many pathogenic plant fungi and against all the bacteria tested [74]. The antimicrobial activity of the methanolic extract of studied Spirulina has been attributed to the presence of functional lipids, mainly γ-linolenic acid, and an antibiotically active fatty acid [77]. In fact, lipids kill microorganisms (bacteria, fungi, and yeasts) by reaching the bacterial membrane and causing their disintegration [78]. Indeed, they are disrupting the extensive meshwork of peptidoglycans in the cell wall without visible changes. γ-Linolenic acid and other fatty acids known for their antimicrobial activity are highly presented in Spirulina. Study [79] showed that the synergistic effect between these fatty acids is involved in their antimicrobial activity [80].


Bacillus subtilis++++++++
Staphylococcus aureus++++++++
Escherichia coli++++++++
Micrococcus luteus++++++++

Aspergillus niger++++++++
Coriolus versicolor+++++++

4. Conclusions

Given its chemical composition, rich nutritional value, and antimicrobial and antioxidant activities, the Moroccan Spirulina has important nutraceutical potential. Furthermore, pharmacochemical, experimental, and clinical studies on the Moroccan Spirulina are required to identify its mechanism of action as a complement of traditional pharmacopeia.

Data Availability

The data used to support the findings of this study are included within the article.

Conflicts of Interest

The authors declare that they have no conflicts of interest.


The authors are grateful to the National Center for Agricultural Research, a Research Unit on Agri-Food Technology and Quality (Rabat); University Center for Analysis, Expertise, Transfer of Technology and Incubation, University Ibn Tofaïl, Kénitra; Research Laboratory of Biotechnology and Biomolecule Engineering (ERBGB), Faculty of Science and Technology, Abdelmalek Essaadi University, Tangier; and Center of Forest Research, at Research Unit of Medicines and Microbiology, Rabat, Morocco, for the research facilities. The algal supplier “Spirulina-Berbère” (Morocco) is thanked for providing samples.


  1. C. E. Blank and P. Sãnchez-baracaldo, “Timing of morphological and ecological innovations in the cyanobacteria-a key to understanding the rise in atmospheric oxygen,” Geobiology, vol. 8, no. 1, pp. 1–23, 2010. View at: Publisher Site | Google Scholar
  2. D. B. Stengel, S. Connan, and Z. A. Popper, “Algal chemodiversity and bioactivity: sources of natural variability and implications for commercial application,” Biotechnology Advances, vol. 29, no. 5, pp. 483–501, 2011. View at: Publisher Site | Google Scholar
  3. F. Shahidi, “Nutraceuticals and functional foods: whole versus processed foods,” Trends in Food Science and Technology, vol. 20, no. 9, pp. 376–387, 2009. View at: Publisher Site | Google Scholar
  4. M. F. P. Navacchi, J. C. M. De Carvalho, K. P. Takeuchi, and E. D. G. Danesi, “Development of cassava cake enriched with its own bran and Spirulina platensis,” ActaScientiarum Technology (Maringa), vol. 34, no. 4, pp. 465–472, 2012. View at: Publisher Site | Google Scholar
  5. P. Spolaore, C. Joannis-Cassan, E. Duran, and A. Isambert, “Commercial applications of microalgae,” Journal of Bioscience and Bioengineering, vol. 101, no. 2, pp. 87–96, 2006. View at: Publisher Site | Google Scholar
  6. O. Pulz and W. Gross, “Valuable products from biotechnology of microalgae,” Applied Microbiology and Biotechnology, vol. 65, no. 6, pp. 635–648, 2004. View at: Publisher Site | Google Scholar
  7. H. Li, K. Cheng, C. Wong, K. Fan, F. Chen, and Y. Jiang, “Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae,” Food Chemistry, vol. 102, no. 3, pp. 771–776, 2007. View at: Publisher Site | Google Scholar
  8. G. Chamorro, M. Saläzar, K. G. Araujo, C. P. Dos Santos, G. Ceballos, and L. F. Castillo, “Update on the pharmacology of Spirulina (Arthrospira), and conventional food,” Archivos Latinoamericanos de Nutrición, vol. 52, no. 3, pp. 232–240, 2002. View at: Google Scholar
  9. R. Balasubramani, S. K. Gupta, W. Cho et al., “Microalgae potential and multiple roles-current progress and future prospects-an overview,” Sustainability, vol. 8, no. 12, pp. 545-546, 2016. View at: Publisher Site | Google Scholar
  10. E. W. Becker, “Micro-algae as a source of protein,” Biotechnology Advances, vol. 25, no. 2, pp. 207–210, 2007. View at: Publisher Site | Google Scholar
  11. M. E. Gershwin and A. Belay, “Spirulina in human nutrition and health,” Journal of Applied Phycology, vol. 21, no. 6, pp. 747-748, 2009. View at: Publisher Site | Google Scholar
  12. H. M. Amaro, A. C. Guedes, and F. X. Malcata, “Science against microbial pathogens: communicating current research and technological advances,” in Antimicrobial Activities of Microalgae: An Invited Review, A. Méndez-Vilas, Ed., pp. 1272–1280, 2011. View at: Google Scholar
  13. R. Balasubramani, S. K. Gupta, W. Cho et al., “Microalgae potential and multiple roles-current progress and future prospects-an overview,” Sustainability, vol. 8, no. 12, pp. 545-546, 2016. View at: Google Scholar
  14. T. M. Mata, A. A. Martins, and N. S. Caetano, “Microalgae for biodiesel production and other applications: a review,” Renewable and Sustainable Energy Reviews, vol. 14, no. 1, pp. 217–232, 2010. View at: Publisher Site | Google Scholar
  15. AACC, American Association of Cereal Chemists Approved Methods, AACC, Saint Paul, MN, USA, 8th edition, 1983.
  16. B. R. Brunner and R. D. Freed, “Oat grain β-glucan content as affected by nitrogen level, location, and year,” Crop Science, vol. 34, no. 2, pp. 473–476, 1994. View at: Publisher Site | Google Scholar
  17. AOAC Association of Official Analytical Chemists, Methods of Analysis for Nutrition Labeling, Airlington, TX, USA, 1993.
  18. P. J. Van Soest, J. B. Robertson, and B. A. Lewis, “Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition,” Journal of Dairy Science, vol. 74, no. 10, pp. 3583–3597, 1991. View at: Publisher Site | Google Scholar
  19. M. Rinne, P. Huhtanen, and S. Jaakkola, “Grass maturity effects on cattle fed silage-based diets. 2. Cell wall digestibility, digestion and passage kinetics,” Animal Feed Science and Technology, vol. 67, no. 1, pp. 19–35, 1997. View at: Publisher Site | Google Scholar
  20. H. D. Chapman and P. F. Pratt, “Methods of analysis for soils, plants and waters,” in Book Review, Soil Sc, vol. 93, no. 1, pp. 162–165, 1962. View at: Google Scholar
  21. M. Pinta, “Spectrométrie d’absorption atomique,” in Tom II, Application à l’Analyse Chimique, 1971. View at: Google Scholar
  22. L. Duchoňová, P. Polakovičová, M. Rakická, and E. Šturdík, “Characterization and selection of cereals for preparation and utilization of fermented fiber-beta-glucan product,” Journal of Microbiology, Biotechnology and Food Sciences, vol. 2, no. 1, pp. 1384–1404, 2013. View at: Google Scholar
  23. V. L. Singleton and J. A. Rossi, “Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents,” American Journal of Enology and Viticulture, vol. 16, pp. 144–153, 1965. View at: Google Scholar
  24. T. Bahorun, B. Gressier, F. Trotin et al., “Oxygen species scavenging activity of phenolic extract from Hawthorn fresh plant organs and pharmaceutical preparations,” Arzneinmittel-Forschung, vol. 46, no. 11, pp. 1086–1089, 1996. View at: Google Scholar
  25. Z. Liu and H. Nakano, “Antibacterial activity of spice extracts against food-related bacteria,” Journal of the Faculty of the Applied Biological Science, vol. 35, pp. 181–190, 1996. View at: Google Scholar
  26. D. Lopes-Lutz, D. S. Alviano, C. S. Alviano, and P. P. Kolodziejczyk, “Screening of chemical composition, antimicrobial and antioxidant activities of Artemisia essential oils,” Phytochemistry, vol. 69, no. 8, pp. 1732–1738, 2008. View at: Publisher Site | Google Scholar
  27. A. Tantaoui-Elaraki, A. Errifi, B. Benjilali, and N. Lattaoui, “Antimicrobial activity of four chemically different essential oils,” RivistaItaliana EPPOS, vol. 6, pp. 13–23, 1992. View at: Google Scholar
  28. A. Remmal, T. Bouchikhi, K. Rhayour, M. Ettayebi, and A. Tantaoui-Elaraki, “Improved method for the determination of antimicrobial activity of essential oils in agar medium,” Journal of Essential Oil Research, vol. 5, no. 2, pp. 179–184, 1993. View at: Publisher Site | Google Scholar
  29. B. Satrani, A. Farah, and M. Fechtal, “Composition chimique et activité antimicrobienne des huiles essentielles de Saturejacalaminthe et Satureja alpine du Maroc,” Annales des Falsifications et de l’Expertise Chimique et Toxicologique, vol. 94, no. 956, pp. 241–250, 2001. View at: Google Scholar
  30. M. A. B. Habib and M. Parvin, “A review on culture, production and use of Spirulina as food for humans and feeds for domestic animals and fish,” FAO Fisheries and Aquaculture, pp. 10–34, 2008. View at: Google Scholar
  31. F. F. Madkour, A. E.-W. Kamil, and H. S. Nasr, “Production and nutritive value of Spirulina platensis in reduced cost media,” The Egyptian Journal of Aquatic Research, vol. 38, no. 1, pp. 51–57, 2012. View at: Publisher Site | Google Scholar
  32. L. Gouveia, A. P. Batista, I. Sousa, A. Raymundo, and N. M. Bandarra, Microalgae in Novel Food Product, 2008.
  33. E. N. Dewi, U. Amalia, and M. Mel, “The effect of different treatments to the amino acid contents of micro algae Spirulina sp,” Aquatic Procedia, vol. 7, pp. 59–65, 2016. View at: Publisher Site | Google Scholar
  34. E. Christaki, P. Florou-Paneri, and E. Bonos, “Microalgae: a novel ingredient in nutrition,” International Journal of Food Sciences and Nutrition, vol. 62, no. 8, pp. 794–799, 2011. View at: Publisher Site | Google Scholar
  35. E. W. Becker, “Microalgae for human and animal nutrition,” in Handbook of Microalgal Culture, pp. 461–503, John Wiley & Sons, Ltd, Hoboken, NJ, USA, 2013. View at: Google Scholar
  36. K. H. Wong and P. C. K. Cheung, “Nutritional evaluation of some subtropical red and green seaweeds,” Food Chemistry, vol. 71, no. 4, pp. 475–482, 2000. View at: Publisher Site | Google Scholar
  37. J. Reboleira, R. Freitas, S. Pinteus et al., “Brown seaweeds,” in Nonvitamin and Nonmineral Nutritional Supplements, pp. 171–176, 2019. View at: Publisher Site | Google Scholar
  38. M. G. Morais, C. C. Reichert, F. Dalcanton, A. J. Durante, L. F. Marins, and J. A. V. Costa, “Isolation and characterization of a new Arthrospira sp.,” Zeitschrift für Naturforschung C, vol. 63, no. 1-2, pp. 144–150, 2008. View at: Publisher Site | Google Scholar
  39. H. K. Maehre, L. Dalheim, G. K. Edvinsen, E. O. Elvevoll, and I. J. Jensen, “Protein determination method matters,” Foods, vol. 7, no. 1, p. 5, 2018. View at: Google Scholar
  40. C. P. Wolk, “Physiology and cytological chemistry blue-green algae,” Bacteriological Reviews, vol. 37, pp. 32–101, 1973. View at: Google Scholar
  41. S.M. Ametamey, M. Bruehlmeier, S. Kneifel et al., “PET studies of 18 F-memantine in healthy volunteers,” Nuclear Medicine and Biology, vol. 29, pp. 227–231, 2002. View at: Publisher Site | Google Scholar
  42. A. Belay, “Spirulina (Arthrospira): production and quality assurance,” in Spirulina in Human Nutrition and Health, M. E. Gershwin and A. Belay, Eds., pp. 16–40, CRC Press, Boca Raton, FL, USA, 2008. View at: Google Scholar
  43. J. Ortiz, E. Uquiche, P. Robert, N. Romero, V. Quitral, and C. Llantén, “Functional and nutritional value of the Chilean seaweeds Codium fragile, Gracilaria chilensis and Macrocystis pyrifera,” European Journal of Lipid Science and Technology, vol. 111, no. 4, pp. 320–327, 2009. View at: Publisher Site | Google Scholar
  44. J. Lunn and J. L. Buttriss, “Carbohydrates and dietary fibre,” Nutrition Bulletin, vol. 32, no. 1, pp. 21–64, 2007. View at: Publisher Site | Google Scholar
  45. O. Tokusoglu and M. K. Unal, “Biomass nutrient profiles of three microalgae: Spirulina platensis, Chlorella vulgaris, and Isochrisisgalbana,” Journal of Food Science, vol. 68, no. 4, pp. 1144–1148, 2003. View at: Google Scholar
  46. J. Volkman and M. Brown, “Nutritional value of microalgae and applications,” in Algal Cultures, Analogues of Blooms and Applications, D. V. Subba Rao, Ed., pp. 407–457, CABI, Wallingford, UK, 2006. View at: Google Scholar
  47. P. Rupẽrez and F. Saura-Calixto, “Dietary fibre and physicochemical properties of edible Spanish seaweeds,” European Food Research and Technology, vol. 212, no. 3, pp. 349–354, 2001. View at: Publisher Site | Google Scholar
  48. WHO, Global Strategy on Diet, Physical Activity and Health, WHO, Geneva, Switzerland, 2004.
  49. K.-Y. Show, D.-J. Lee, and J.-S. Chang, “Algal biomass dehydration,” Bioresource Technology, vol. 135, pp. 720–729, 2013. View at: Publisher Site | Google Scholar
  50. N. Nicolucci, A. Monegato, and F. De Poli, “Produzioneindustriale di carta ottenuta dalle alghe in esuberonellalaguna di Venezia,” Cellulosa e Carta, vol. 5-6, pp. 41–47, 1994. View at: Google Scholar
  51. C. Dawczynski, R. Schubert, and G. Jahreis, “Amino acids, fatty acids, and dietary fibre in edible seaweed products,” Food Chemistry, vol. 103, no. 3, pp. 891–899, 2007. View at: Publisher Site | Google Scholar
  52. P. Burtin, “Nutritional value of seaweeds,” Electronic Journal of Environmental, Agricultural and Food Chemistry, vol. 2, pp. 498–503, 2003. View at: Google Scholar
  53. E. Marinho-Soriano, P. C. Fonseca, M. A. A. Carneiro, and W. S. C. Moreira, “Seasonal variation in the chemical composition of two tropical seaweeds,” Bioresource Technology, vol. 97, no. 18, pp. 2402–2406, 2006. View at: Publisher Site | Google Scholar
  54. P. V. S. Rao, V. A. Mantri, and K. Ganesan, “Mineral composition of edible seaweed Porphyra vietnamensis,” Food Chemistry, vol. 102, no. 1, pp. 215–218, 2007. View at: Publisher Site | Google Scholar
  55. S. M. Tibbetts, J. E. Milley, and S. P. Lall, “Chemical composition and nutritional properties of freshwater and marine microalgal biomass cultured in photobioreactors,” Journal of Applied Phycology, vol. 27, no. 3, pp. 1109–1119, 2015. View at: Publisher Site | Google Scholar
  56. S. Gebhardt and R. G. Thomas, Nutritive Value of Foods, vol. 95, U.S. Department of Agriculture, Agricultural Research Service, Nutrient Data Laboratory, Beltsville, MD, USA, 2002.
  57. P. Ruperez, “Mineral content of edible marine seaweeds,” Food Chemistry, vol. 79, no. 1, pp. 23–26, 2002. View at: Publisher Site | Google Scholar
  58. A. Belay, “Spirulina (Arthrospira) production and quality assurance,” in Spirulina in Human Nutrition and Health, E. Gershwin and A. Belay, Eds., pp. 1–23, CRC Press, Taylor & France Group, Boca Raton, FL, USA, 2008. View at: Google Scholar
  59. V. Kumar, A. K. Bhatnagar, and J. N. Srivastava, “Antibacterial activity of crude extracts of Spirulina platensis and its structural elucidation of bioactive compound,” Journal of Medicinal Plants Research, vol. 5, no. 32, pp. 7043–7048, 2011. View at: Google Scholar
  60. P. Kaushik and A. Chauhan, “In vitro antibacterial activity of laboratory grown culture of Spirulina platensis,” Indian Journal of Microbiology, vol. 48, no. 3, pp. 348–352, 2008. View at: Publisher Site | Google Scholar
  61. T. Hirata, M. Tanaka, M. Ooike et al., “Antioxidant activities of phycocyanin prepared from Spirulina platensis,” Journal of Applied Phycology, vol. 12, no. 3-5, pp. 435–439, 2000. View at: Publisher Site | Google Scholar
  62. M. Hajimahmoodi, M. A. Faramarzi, N. Mohammadi, N. Soltani, M. R. Oveisi, and N. Nafissi-Varcheh, “Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae,” Journal of Applied Phycology, vol. 22, no. 1, pp. 43–50, 2010. View at: Publisher Site | Google Scholar
  63. F. Ahmed, K. Fanning, M. Netzel, W. Turner, Y. Li, and P. M. Schenk, “Profiling of carotenoids and antioxidant capacity of microalgae from subtropical coastal and brackish waters,” Food Chemistry, vol. 165, pp. 300–306, 2014. View at: Publisher Site | Google Scholar
  64. M. G. Morais, B. S. Vaz, E. G. Morais, and J. A. V. Costa, “Biologically active metabolites synthesized by microalgae,” BioMed Research International, vol. 2015, Article ID 835761, 15 pages, 2015. View at: Publisher Site | Google Scholar
  65. S. Connan and D. B. Stengel, “Impacts of ambient salinity and copper on brown algae: 2. Interactive effects on phenolic pool and assessment of metal binding capacity of phlorotannin,” Aquatic Toxicology, vol. 104, no. 1-2, pp. 1–13, 2011. View at: Publisher Site | Google Scholar
  66. H. Safafar, J. van Wagenen, P. Møller, and C. Jacobsen, “Carotenoids, Carotenoids, phenolic compounds and tocopherols contribute to the antioxidative properties of some microalgae species grown on industrial wastewater,” Marine Drugs, vol. 13, no. 12, pp. 7339–7356, 2015. View at: Publisher Site | Google Scholar
  67. R. A. Kepekçi and S. D. Saygideger, “Enhancement of phenolic compound production in Spirulina platensis by two-step batch mode cultivation,” Journal of Applied Phycology, vol. 24, no. 4, pp. 897–905, 2012. View at: Publisher Site | Google Scholar
  68. I. Jerez-Martel, S. García-Poza, G. Rodríguez-Martel, M. Rico, C. Afonso-Olivares, and J. L. Gómez-Pinchetti, “Phenolic profile and antioxidant activity of crude extracts from microalgae and cyanobacteria strains,” Journal of Food Quality, vol. 2017, Article ID 2924508, 8 pages, 2017. View at: Google Scholar
  69. F. A. Pognussatt, E. M. Del Ponte, J. Garda-Buffon, and E. Badiale-Furlong, “Inhibition of Fusarium graminearum growth and mycotoxin production by phenolic extract from Spirulina sp,” Pesticide Biochemistry and Physiology, vol. 108, pp. 21–26, 2014. View at: Publisher Site | Google Scholar
  70. F. A. Pagnussatt, V. R. De Lima, C. L. Dora, J. A. V. Costa, J.-L. Putaux, and E. Badiale-Furlong, “Assessment of the encapsulation effect of phenolic compounds from Spirulina sp. LEB-18 on their antifusarium activities,” Food Chemistry, vol. 211, no. 211, pp. 616–623, 2016. View at: Publisher Site | Google Scholar
  71. P. Piñero-Estrada, P. Bermejo-Bescos, and A. M. Villar del Fresno, “Antioxidant activity of different fractions of Spirulina platensis protean extract,” II Farmaco, vol. 56, no. 5-7, pp. 497–500, 2001. View at: Publisher Site | Google Scholar
  72. W. L. Chu, Y. W. Lim, A. K. Radhakrishnan, and P. E. Lim, “Protective effect of aqueous extract from Spirulina platensis against cell death induced by free radicals,” BMC Complementary and Alternative Medicine, vol. 10, no. 53, 2010. View at: Publisher Site | Google Scholar
  73. T. W. Agustini, M. Suzery, D. Sutrisnanto, W. F. Ma’ruf, and Hadiyanto, “Comparative study of bioactive substances extracted from fresh and dried Spirulina sp,” Procedia Environmental Sciences, vol. 23, pp. 282–289, 2015. View at: Publisher Site | Google Scholar
  74. M. Hetta, R. Mhmoud, W. El-Senousy, M. Ibrahim, G. El-Taweel, and G. Ali, “Antiviral and antimicrobial activities of Spirulina platensis,” World Journal of Pharmaceutical Sciences, vol. 3, pp. 31–39, 2014. View at: Google Scholar
  75. J. A. Ross and C. M. Kasum, “Dietary flavonoids: bioavailability, metabolic effects, and safety,” Annual Review of Nutrition, vol. 22, no. 1, pp. 19–34, 2002. View at: Publisher Site | Google Scholar
  76. C. M. M. Sousa, H. R. Silva, G. M. Vieira Jr. et al., “Fenóis totais e atividade antioxidante de cinco plantas medicinais,” Química Nova, vol. 30, no. 2, pp. 351–355, 2007. View at: Publisher Site | Google Scholar
  77. C. Xue, Y. Hu, H. Saito et al., “Molecular species composition of glycolipids from Sprirulina platensis,” Food Chemistry, vol. 77, no. 1, pp. 9–13, 2002. View at: Publisher Site | Google Scholar
  78. Y. Shai, “Mode of action of membrane active antimicrobial peptides,” Biopolymers, vol. 66, no. 4, pp. 236–248, 2002. View at: Publisher Site | Google Scholar
  79. M. F. Ramadan, M. M. S. Asker, and Z. K. Ibrahim, “Functional bioactive compounds and biological activities of Spirulina platensis lipids,” Czech Journal of Food Sciences, vol. 26, no. 3, pp. 211–222, 2008. View at: Publisher Site | Google Scholar
  80. J. A. Mendiola, L. Jaime, S. Santoyo et al., “Screening of functional compounds in supercritical fluid extracts from Spirulina platensis,” Food Chemistry, vol. 102, no. 4, pp. 1357–1367, 2007. View at: Publisher Site | Google Scholar

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