Hindawi

Journal of Food Quality

Volume 2019, Article ID 3707219, 11 pages
https://doi.org/10.1155/2019/3707219

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

Rajaa Seghiri ,1 Mourad Kharbach,2 and Azzouz Essamri1

1
Laboratory of Agro-Resources, Polymers and Process Engineering (LAR2PE), Department of Chemistry, Faculty of Sciences,
Ibn Tofaı̈l University, B.P. 133, 14000 Kenitra, Morocco
2
Biopharmaceutical and Toxicological Analysis Research Team, Laboratory of Pharmacology and Toxicology,
Faculty of Medicine and Pharmacy, University Mohammed V, Rabat, Morocco

Correspondence should be addressed to Rajaa Seghiri; rajaa.seghiri@gmail.com

Received 25 January 2019; Revised 28 April 2019; Accepted 20 May 2019; Published 3 July 2019

Academic Editor: Francisca Hernández

Copyright © 2019 Rajaa Seghiri et al. This 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.
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 such as pasta, gums, and beverages [5]. On the contrary,

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 recogni-
tion 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,
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 im-
portant 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 Aphanizome-
non 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.
2 Journal of Food Quality
Spirulina is an abundant source of nutritious compo-
sition, including protein, vitamins, lipids, fibers, minerals,
carbohydrates, and some of natural pigments [10]. Spirulina
was recognized as a safe supplement (GRAS) without tox-
icological 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 ac-
tivities were evaluated.
2. Materials and Methods
2.1. Raw Materials. Spirulina platensis (Arthrospira pla-
tensis) 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 com-
pany’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 hemi-
cellulose was calculated according to the method
in [19].
Mineral composition: macroelements including K+ and
Na+ contents were determined using a flame pho-
tometer, while Mg2+ and Ca2+ contents were de-
termined using complexometric titration. On the
contrary, phosphorus content was measured by using
the acidified solution reaction of ammonium molyb-
date 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 com-
position data. Energy (kcal) was calculated according to
the following equation:
E(kcal) � CP × 4 + CHO × 4 + fat × 9. (1)
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
Journal of Food Quality
(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 Com-
position. The Agilent 1100 high-performance liquid chro-
matography (HPLC) system (Agilent Technologies, Inc.,
Wilmington, DE, USA) is composed of a diode array de-
tector (DAD) (G1315B), an autosampler (G1330B), and a
binary pump (G1312A). The mass spectrometer (MS) de-
tector 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 modifica-
tions. 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.
3
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:
% inhibition � [(Abs of control – Abs of test sample)
÷ Abs of control] × 100 %.
(2)
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 con-
sidered 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.
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
4 Journal of Food Quality
Table 1: Global nutritional analysis of Spirulina (Morocco) (% of
dry matter).
Elements Percentage (%)b Other micro/macroalgae
Moisturea (%) 12.66 ± 1.7 <9% [48]
7.4–10.4% [5, 37, 54]
Ash (%) 14.56 ± 0.74
4–20% [55, 56]
60–71 [5, 36, 37],
Protein (%) 76.65 ± 0.15 6–71% [39–45]
3–47% [46, 47]
6–13% [5, 37]
Lipids (%) 2.45 ± 0.82 >60% [39–45]
>5% [46, 47]
CF (%) 4.07 ± 1.42 1.36–7.73% [53]
15–25% [5, 36, 37]
Carbohydrates (%)c 6.46 ± 0.32 10–27% [39–45]
20–68% [46, 47]
Energy (kcal/100 g) 436.18 ± 2.29 ND
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.
countries [31, 32], with its amino acid composition of
aspartic acid, glutamic acid, serine, glycine, histidine, argi-
nine, 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]. Fur-
thermore, several studies have demonstrated that the protein
content of microalgae varied according to species, envi-
ronmental 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 poly-
unsaturated fatty acids (PUFAs), mainly c-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 Spir-
ulina 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 con-
ditions 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 de-
termination of crude fiber (CF, lignocellulose complex) and
some polysaccharides of fibrous nature which would be
identified further by future studies using highly sophisti-
cated 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].
Journal of Food Quality
Table 2: Mineral composition of Spirulina (Morocco) (mg/100g dw).
Elements
P 10088.33 ± 5766.88
Na
Minerals (mg/100 g dw) K 2501.66 ± 4.22
Ca
Mg
Fe
Zn
Trace elements (mg/100 g dw)
Cu
Mn
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 Zar-
rouk’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.
3.2. Microbiological Analysis. The edible product was ex-
posed to all contamination vectors. The microbial moni-
toring 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 ed-
ible 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, specifi-
cally 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 bio-
mass by the company were moderately satisfactory
according to the European Union and World Health Or-
ganization 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
5
Spirulina studied Other microalgae [55]
1700–3000
14004 ± 397.55 7000–1100
600–1200
6000 ± 4.66 300–2100
100.33 ± 1.77 100–1100
80.66 ± 1.77 100–700
5 ± 0.66 23.9–370
1.22 ± 0.66 1.2–65
1.56 ± 0.11 3.7–59.2
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 al-
kalinity of the Spirulina environment is normally an ex-
cellent barrier to contamination, whether by bacteria, fungi,
or algae. Furthermore, certain substances of both intracel-
lular 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).
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 sec-
ondary 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
6 Journal of Food Quality

Table 3: Microbiological quality of edible Spirulina (cfu/ml).

All aerobic mesophilic Total Fecal Sulfito-reducer Yeasts and
Pathogens Staphylococcus E. coli Salmonella
flora coliforms coliforms bacteria molds
Bacterial
208 93 26 ND ND 14 4.15 ND
count
EU
105 Absent Absent No data 104 104 Absent Absent
standard
No
WHO No data No data No data No data 103 Absent
data
EU, European Union [41]; WHO, World Health Organization [42]; ND: not detected.

0.35
Nutraceutical value 0.3
0.25
0.2
Nutritional 0.15
composition
0.1
0.05
Biological
Mineral assay 0
activities
Functional food:
TFC TPC
Spirulina sp.
Figure 2: Total phenolic content (TPC) and total flavonoid content
(TFC) of the methanolic extract of Spirulina expressed as μg mg
Physicochemical Food safety GAE/g DW and mg QE/g DE, respectively (n  3).
analysis control

Figure 1: Crosstalk between nutritional and physicochemical
properties and bioactivities in the functional food Spirulina species.
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 chro-
matographic 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 frag-
mentations) 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].
3.3.3. Antioxidant Bioactivity Analysis. The total antioxi-
dant capacity (TAC) of the methanolic extract was de-
termined 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 pre-
formed free radical by antioxidants and EC50 (concen-
tration 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 com-
pounds. 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 an-
tioxidant 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 in-
hibition [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
Journal of Food Quality 7

Table 4: Phenolic and flavonoid compounds determined in the Spirulina-evaluated samples (mg/kg).
HPLC-ESI/MS (m/z)
Phenolic acids Spirulina Molecular formula Molecular weight (M)
RT (min) [M-H]−
Quinic acid 844.17 ± 42.21 C7H12O6 192.167 0.51 191.120
Citric acid 64.06 ± 3.20 C6H8O7 192.123 0.63 191.102
Pyrogallol 0.42 ± 0.02 C6H6O3 126.111 0.64 125.024
Succinic acid 1122.88 ± 56.14 C4H6O4 118.088 0.65 117.018
Gallic acid 2.13 ± 0.11 C7H6O5 170.022 0.66 168.90
Chlorogenic acid 0.86 ± 0.04 C16H18O9 354.311 0.83 353.202
3,4-Hydroxybenzoic acid 687.07 ± 34.35 C7H6O4 154.121 0.95 153.010
4-Hydroxybenzoic acid 1.07 ± 0.05 C7H6O3 138.122 1.30 137.050
Catechin 584.53 ± 29.22 C15H14O6 290.271 1.63 289.064
Vanillic acid 16.24 ± 0.81 C8H8O4 168.148 2.12 167.036
4-Hydroxycinnamic acid 0.12 ± 0.01 C9H8O3 164.160 2.21 163.042
Rutin 0.93 ± 0.05 C27H30O16 610.153 2.63 609.1
3-Hydroxycinnamic acid 0.15 ± 0.01 C9H8O3 164.160 2.98 163.042
Ferulic acid 0.48 ± 0.02 C10H10O4 194.186 3.12 193.050
Quercetin 0.01 ± 0.00 C15H10O7 302.238 3.48 301.000
2-Hydroxycinnamic acid 0.31 ± 0.02 C9H8O3 164.160 3.65 163.042
Salicylic acid 0.08 ± 0.003 C7H6O3 138.122 3.68 137.025
Rosmarinic acid 0.18 ± 0.01 C18H16O8 360.318 4.01 359.054
Resveratrol 0.10 ± 0.005 C14H12O3 228.247 5.83 227.072
Quercitrin 0.04 ± 0.00 C21H20O11 448.38 5.99 447.120
4-Hydroxycoumarin ND C9H8O3 164.160 ND 163.042
Aesculin ND C15H16O9 340.284 ND 339.072
Epigallocatechin gallate ND C22H18O11 458.375 ND 457.078
Esculetin ND C9H6O4 178.143 ND 177.018
Kaempferol ND C15H10O6 286.239 ND 285.040
Luteolin ND C15H10O6 286.239 ND 285.040
Malic acid ND C4H6O5 134.087 ND 133.014
Syringic acid ND C9H10O5 198.174 ND 197.045
3-Hydroxybenzoic acid ND C7H6O3 138.122 ND 137.025
Benzoic acid ND C7H6O2 122.123 ND 121.031
Caffeic acid ND C9H8O4 180.159 ND 179.035
Epicatechin ND C15H14O6 290.271 ND 289.064
Hesperetin ND C16H14O6 302.282 ND 301.015
Hesperidin ND C28H34O15 610.565 ND 609.172
Naringenin ND C15H12O5 272.256 ND 271.061
Naringin ND C27H32O14 580.539 ND 579.173
Pyrocatechol ND C6H6O2 110.112 ND 109.028
Sinapic acid ND C11H12O5 224.212 ND 223.061
Tannic acid ND C76H52O46 1701.206 ND 1700.080
ND: not detected.

antioxidant compounds in the methanol extract was re-
sponsible 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 nu-
tritional quality and increases food toxicity. The anti-
microbial 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 an-
tifungal activity against Coriolus versicolor, with a min-
imum 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 re-
ported 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 c-linolenic acid, and
an antibiotically active fatty acid [77]. In fact, lipids kill
microorganisms (bacteria, fungi, and yeasts) by reach-
ing the bacterial membrane and causing their disinte-
gration [78]. Indeed, they are disrupting the extensive
meshwork of peptidoglycans in the cell wall without
visible changes. c-Linolenic acid and other fatty acids
known for their antimicrobial activity are highly pre-
sented in Spirulina. Study [79] showed that the synergistic
effect between these fatty acids is involved in their anti-
microbial activity [80].
8 Journal of Food Quality

70
y = 27.785x – 21.67
R2 = 0.9242

Percentage of radical-scavenging activity

60

50

40

30

20

10

0
25 50 100
Concentration (μg/ml)
Methanolic extract
Figure 3: Percentage radical scavenging of the methanolic extract of Spirulina as per DPPH assay-expressed activity (n  3) as a function of
concentration of the extract.

Table 5: Inhibitory volumes and minimum inhibitory concentrations of the methanolic extract of Spirulina (Morocco).
Concentration 1/100 1/250 1/500 1/1000 1/2000 1/3000 1/5000 Control
(mg/ml) 0.001 0.0004 0.002 0.001 0.00005 0.000033 0.00002 0
Bacteria
Bacillus subtilis + + + + + + + +
Staphylococcus aureus + + + + + + + +
Escherichia coli + + + + + + + +
Micrococcus luteus + + + + + + + +
Fungi
Aspergillus niger + + + + + + + +
Coriolus versicolor − + + + + + + +

4. Conclusions Ibn Tofaı̈l, Kénitra; Research Laboratory of Biotechnology

and Biomolecule Engineering (ERBGB), Faculty of Science
Given its chemical composition, rich nutritional value, and and Technology, Abdelmalek Essaadi University, Tangier;
antimicrobial and antioxidant activities, the Moroccan and Center of Forest Research, at Research Unit of Medi-
Spirulina has important nutraceutical potential. Further- cines and Microbiology, Rabat, Morocco, for the research
more, pharmacochemical, experimental, and clinical studies facilities. The algal supplier “Spirulina-Berbère” (Morocco)
on the Moroccan Spirulina are required to identify its is thanked for providing samples.
mechanism of action as a complement of traditional
pharmacopeia.
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