Open Access
Issue
OCL
Volume 25, Number 5, September-October 2018
Article Number D505
Number of page(s) 6
Section Lipids and cosmetics / Lipides et cosmétiques
DOI https://doi.org/10.1051/ocl/2018054
Published online 19 October 2018

© N. Terme et al., Published by EDP Sciences, 2018

Licence Creative Commons
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

1 Introduction

Macro-algae or seaweed are photosynthetic-like plants that form biomass in intertidal zones and at the seabed. More than 10 000 species are identified and classified in three phyla based on their pigmentation. The Rhodophyta phylum contains the red seaweeds, the Chlorophyta phylum corresponds to the green seaweeds and the Phaeophyta to the brown seaweeds. According to the literature (FAO, 2017), the total weight of commercial seaweeds and aquatic plants in the world was 30.5 million tons in 2015, representing a $ 4 billion market. 96% of these species are harvested from aquaculture and are mainly used for the hydrocolloid extraction (FAO, 2016).

Seaweeds are a source of bioactives for cosmetics. Indeed, some seaweeds or seaweed extracts possess an INCI name and are used for their properties. Red seaweeds from Chondrus, Palmaria or Gelidium genera and green seaweeds like Ulva or Enteromorpha are used for emollient, humectant, masking, soothing, smoothing or for skin conditioning and skin protecting properties (Bedoux et al., 2014). The main seaweeds used in cosmetics are brown seaweeds especially from the Laminariaceae and Fucaceae families.

Bioactive compounds from seaweeds are identified as polysaccharides, minerals, proteins, fibres, phenolic compounds, vitamins or lipids. The lipid family includes fats, waxes, sterols, fat-soluble vitamins, glycerolipids, phospholipids, glycolipids and others (Holdt and Kraan, 2011). Usually, the study of seaweed lipidome consists of a total lipid content determination and fatty acid profiling. The major lipid roles involve energy storage, including carbon storage (Reed et al., 1999), structural composition of cellular and intracellular membranes, and cell signalling (Thompson, 1996). The seaweed total lipid content is lower compared to terrestrial plants (Darcy-Vrillon, 1993) or microalgae (Mubarak et al., 2015). The total lipid content is generally established between 1 and 8% dry weight (dw) of seaweeds with a wide variation between species (Melo et al., 2015). However, lipids from seaweeds have a vast array of activities and are possible sources of active compounds due to the large amount of seaweeds on the seaside, the possibility of aquaculture and the biodiversity (Miyashita et al., 2013).

Seaweed lipids can be separated in different classes according to their chemical structures. Lipid classes consist of non-polar lipids, glycolipids and phospholipids as found in plants. Seaweeds contain also betaine and some unusual lipids. The main source of lipids in seaweeds is not well determined. Phospholipids or glycolipids are defined depending on studies as being the major sources of lipid fractions (LeTutour, 1990; Murata and Nakazoe, 2001; Bhaskar et al., 2005; Khotimchenko, 2005). Specific activities have been described for some lipid classes or some lipid molecules. Non-polar lipids consist in hydrocarbons, carotenoids, sterols and glycerolipids. Carotenoids, mainly β-carotene, lutein and violaxanthin in red and green seaweeds and fucoxanthin in brown seaweeds (Holdt and Kraan, 2011), operate both as light energy harvesters and as antioxidants by inactivating reactive oxygen species formed by air and light exposures (von-Elbe and Schwartz, 1996). Sterols, mainly cholesterol in Rhodophyta, fucosterol in Phaeophyta, clionasterol and isofucosterol in Chlorophyta (Kumari et al., 2013) are known to have nutritional benefits on health as they possess antioxidant or anti-inflammatory activities (Kim and Van Ta, 2011) comparable to those obtained from nuts and seeds (Phillips et al., 2005). Non-polar lipid fraction contributes to antioxidant activities through carotenoids, sterols and terpenoids (Okuzumi et al., 1993; Yan et al., 1999; Plaza et al., 2008; Jassbi et al., 2013). Glycolipids are glycosylated derivatives of glycerolipids and derivatives of ceramides. Glycolipids play an important role in cell protection against chemical stress, in membrane bilayer stabilization and they act as markers for cellular recognition (Holdt and Kraan, 2011; Boudière et al., 2014). Phospholipids incorporate two main structures, glycerophospholipids and sphingophospholipids. Glycerolipids, glycolipids, phospholipids and betaine lipids are fatty acid providers. The chain length and degree of unsaturation in seaweeds are higher than those of plants (Kumari et al., 2013). The lipid activity on bacteria, fungi, virus and parasites may be due to fatty acids (Desbois and Smith, 2010). Indeed, fatty acids inhibit enzyme activities, disrupt the electron transport chain and oxidative phosphorylation, and interfere with cellular energy production in microbes. They also damage nutrient uptake, generate peroxidation and auto-oxidation degradation products or direct lyse bacterial cells (Lee et al., 2009; Vedhagiri et al., 2009; Plouguerné et al., 2013). Many fatty acids demonstrate good antioxidant activities (Henry et al., 2002). Furthermore, pigments, polyunsaturated fatty acids, lutein and glycolipids isolated from seaweeds demonstrate activities on pro-inflammatory pathways by inhibition of nitric oxide or icosanoid production in cells (Ishihara et al., 1998; Banskota et al., 2014a, b; Lopes et al., 2014). Thus, according to the literature, all the lipid classes demonstrate antioxidant activities.

Interest in employing natural antioxidants is encouraged by consumers mainly because of the potential toxic effects of some synthetic antioxidants such as butylated hydroxyanisole, butylated hydroxytoluene or tert-butylhydroquinone (Safer, 1999). Free radical and reactive oxygen species induce cutaneous damages like early aging, inflammatory disorders or skin cancers. The use of antioxidant compounds in cosmetics aims to avert and control oxidative skin damages (Vertuani et al., 2003). These compounds can act on aging processes by different mechanisms like reductive capacity, binding of transition metal ion catalysts or radical scavenging (Zubia et al., 2007).

General procedures for lipid extraction correspond to solid/liquid methods and employ organic solvents. Generally, a chloroform/methanol/water mixture (2/2/1 v/v/v) is used (Bligh and Dyer, 1959) for lipid extraction. In this method, chloroform dissolves fat, and methanol breaks down lipid protein bonds and inactivates lipase in a monophasic system (Maciel et al., 2016). Water is then added to produce a biphasic system and wash non-lipid compounds. To obtain a good extraction yield, the Bligh and Dyer method must be repeated twice or three times on the same seaweed sample lengthening extraction duration and exposing the lipids extracted to oxidation. The supercritical fluids demonstrate their ability to extract lipids from seaweeds (Grosso et al., 2015). Supercritical carbon dioxide (sc-CO2) is the most common supercritical fluid used due to its low critical pressure and temperature (73.9 bar and 31.1 °C). Moreover, it is non-toxic, non-flammable, cheap, broadly available, chemically inert under numerous conditions, and gaseous at normal pressure and temperature allowing to recover an extract without use of any organic solvent (Careri et al., 2001; Mendes et al., 2003; Macías-Sánchez et al., 2008; Quitain et al., 2013). CO2 prevents the extract from degradation, giving a non-oxidizing atmosphere (Jaime et al., 2007). Furthermore, sc-CO2 has low viscosity and high diffusivity, allowing a faster and deeper penetration into the seaweed particles (Careri et al., 2001; Ali-Nehari et al., 2012). As the majority of CO2 is recycled after extraction, the cost of each extract decreases. Moreover, the transition to the industrial scale is easily conceivable and allows a large scale production of bioactive compounds (Reverchon and De Marco, 2006). sc-CO2 is convenient to extract non-polar compounds and its solubility properties can be modified by adding a safe and polar solvent like ethanol. In a green approach, the production of waste must be avoided (Buschmann et al., 2017). With sc-CO2 with or without ethanol as co-solvent, the solid residue after lipid extraction is not waste, it can be used for the extraction of interesting compounds such as proteins or polysaccharides by other green methods like microwaves, ultrasonic or enzymatic assisted extractions. Thus, the sequence of selective extraction of the compounds leads to total use of the algal biomass. It is the tenet of a bio-refinery approach (Trivedi et al., 2015).

As this extraction method has been little applied to seaweeds (Crampon et al., 2011), the free radical scavenging activity of lipid classes extracted from seaweeds by supercritical carbon dioxide has never been reported. The present study aimed to investigate the free radical scavenging properties of lipid classes extracted from two different seaweeds, Solieria chordalis and Sargassum muticum, from Brittany’s coast according to conventional and eco-friendly methods.

2 Materials and methods

2.1 Lipid class fractions

The lipid class fractions were prepared according to Terme et al. (2017). Briefly, S. chordalis (Rhodophyta, Gigartinales, Solieriaceae) and S. muticum (Phaeophyceae, Fucales, Sargassaceae) were collected on the littoral area of Saint Gildas de Rhuys (47° 29′ 34.0″ N 2° 49′ 51.0″ W, Atlantic coast, France) in October 2017 and in July 2014, respectively. The fresh algae were sorted and cleaned with tap water to remove epiphytes, sediments, organic debris, and macro fauna. The fresh seaweeds were ground to pieces of about 3 mm with a hammer mill, stored at −25 °C and freeze-dried. The lipids of S. chordalis were extracted using chloroform/methanol (1/1 v/v) or supercritical carbon dioxide pure or with 2% or 8% of ethanol. Chloroform/methanol (1/1) and pure supercritical carbon dioxide were applied to S. muticum in order to extract the total lipids. For chloroform/methanol extraction, dry algae were extracted three times at room temperature with the solvent mixture. Extract was then washed with brine, dried over sodium sulphate and evaporated under reduced pressure. For sc-CO2 extraction, in the pilot scale system, the fluid was heated (45 °C) and pressurized (290 bar) to achieve the supercritical state. The supercritical fluid flow was fixed at 10 kg.h−1. The lipid fractionation was conducted onto a silica gel column (silica 60 Å-particle size 20–45 μm – Fisher Scientific, UK) eluted with dichloromethane to isolate neutral lipids, acetone for glycolipids and finally methanol for phospholipids. Fractions were collected and evaporated to dryness.

2.2 Free-radical scavenging activities

DPPH (2,2-diphenyl-1-picrylhydrazyl) radical scavenging activity was determined according to Boulho et al. (2017) with slight modifications. Briefly, 100 μl of each lipid fraction at different concentrations between 1 and 10 mg/ml in methanol was mixed in a 96-well plate with 100 μl of a DPPH solution (0.1 g/l) in methanol prepared just before use. Due to the colour intensity of each fraction, it was necessary to prepare a blank of 100 μl of each sample at the same concentration tested in methanol mixed with 100 μl of methanol. A solution of BHA (butylated hydroxyanisole) at different concentrations range from 1 to 20 μg/ml in methanol (final concentration) was also tested as a positive control. After stirring, the microplate was incubated at 37 °C for 30 min (stationary state). Finally, the absorbance was read at 517 nm by a ThermoScientific Multiscan Go UV-vis apparatus. All the tested solutions (sample and standard) were made in triplicate and the results obtained were expressed as a mean of the percentage of DPPH radical scavenging. The ability to scavenge the DPPH radical was calculated using the equation: where Acontrol is the absorbance of the DPPH solution, Asample is the absorbance of the tested sample (sample + DPPH) and Asample blank is the absorbance of the sample (sample + methanol).

2.3 Statistical analysis

All measurements were made in triplicate. All data are reported as mean ± standard deviation (s.d.). Statistical analyses were by one-way analysis of variance ANOVA and Tukey’s pairwise a posteriori test. All statistical analyses were performed using Past 3.12 (Hammer et al., 2001) at p < 0.05 level.

3 Results and discussion

DPPH reagent has been widely used for measuring the free radical scavenging activities of compounds or extracts. DPPH reagent is scavenged by antioxidant molecules through the donation of a hydrogen forming the reduced diphenylpicrylhydrazine (DPPH-H). The changes in the wavelength of the maximum absorption permit to quantify the scavenging of the radical and it is visually noticeable as a colour change from purple to yellow.

Table 1 indicates the percentage of DPPH radical scavenging activity of lipid classes from S. chordalis according to the method used for lipid extraction at a concentration of 1 mg/ml of lipid class in methanol.

All lipid classes from S. chordalis showed free radical scavenging activities at 1 mg/ml. These activities are lower compared to BHA at 10 μg/ml. The neutral lipids from the chloroform/methanol (CM) extraction exhibited the highest activity (86.6 ± 5.7% of scavenging). This high activity might be due to α-tocopherol, fucosterol or squalene which have been identified in this fraction previously (Kendel et al., 2015) and have been known as antioxidant compounds (Zubia et al., 2007). The activity of neutral lipids was lower for the supercritical carbon dioxide (sc-CO2) extraction with or without co-solvent. However, the scavenging was not significantly different for each extract and was established around 16%. This result suggests that the composition of the neutral lipid fractions is the same whatever the extraction method. As the quantity of neutral lipid extracted increases with the addition of ethanol (Terme et al., 2017), the combination of sc-CO2 and ethanol seems to be the best way to obtain antiradical compounds from the neutral lipid fraction. For glycolipids, the best activity was obtained with the CM extraction (49.3 ± 1.6% of scavenging). The activity observed with the pure supercritical carbon dioxide extraction was twice lower (24.7 ± 1.1% of scavenging) than the one observed with CM extraction. In this case, the addition of ethanol in sc-CO2 produced a less active fraction. However, no significant difference was observed by increasing the amount of ethanol despite an increase of the glycolipid quantity (Terme et al., 2017). This result suggests that sc-CO2 did not efficiently extract antioxidant glycolipids from S. chordalis. The phospholipids extracted by sc-CO2 demonstrated an equivalent activity than the one noticed for the phospholipids extracted using CM. The most active fraction was obtained with sc-CO2 + ethanol 8% with a half more activity than the lipids extracted with CM. As the content of phospholipids decreased when ethanol was added to sc-CO2 (Terme et al., 2017), 8% ethanol in sc-CO2 might extract phospholipids with a greater free radical scavenging activity. Phospholipids with polyunsaturated fatty acids were probably extracted with selectivity as they are known to have antioxidant properties (Henry et al., 2002).

Table 2 indicates the percentage of DPPH radical scavenging activity of lipid classes from S. muticum according to the method used for lipid extraction at a concentration of 1 mg/ml of lipid classes in methanol.

Each lipid class from S. muticum showed a free radical scavenging activity at the 1 mg/ml. The activities are lower compared to BHA at 10 μg/ml. Glycolipids and phospholipids exhibited the best activities for sc-CO2 extraction and the results obtained for these two classes were not significantly different. The activities of glycolipids (50.9 ± 0.8%) and phospholipids (48.4 ± 1.6%) obtained with sc-CO2 were twice as large as that of fractions obtained with CM, 29.6 ± 3.4% and 28.0 ± 4.2%, respectively. Concerning neutral lipids, the results were not significantly different for the two extraction methods and the neutral lipid fraction obtained with sc-CO2 is near than twice less of those obtained for glycolipids and phospholipids. According to our previous results (Terme et al., 2017), the glycolipid and phospholipids fractions represented up to 90% of the lipid fraction from this seaweed. Therefore, the supercritical carbon dioxide is a good method to extract a free radical scavenging fraction from the seaweed S. muticum.

Because of a lack of free radical scavenging data on lipid classes from seaweeds our results cannot be evaluated by comparing with other species or with other extraction methods. However, the results obtained for the lipid classes were in the same range than those obtained from methanol/chloroform extract from other Sargassum species (Matsukawa et al., 1997; Yan et al., 1998; Zubia et al., 2007; Lu et al., 2010). The results obtained for both seaweeds are comparable or greater than those obtained generally for brown or red seaweeds (Zhang et al., 2007; de Alencar et al., 2016). sc-CO2 extracts from Chlorella pyrenoidosa demonstrated free radical scavenging activities between 17.35% and 54.16% at 10 mg/ml (Hu et al., 2007). The DPPH radical scavenging activity increased with the increasing amount of ethanol in supercritical carbon dioxide as we observed for S. chordalis.

Table 1

DPPH radical scavenging activity (%) at 1 mg/ml and EC50 (mg/ml) of the lipid classes obtained from Solieria chordalis according to the extraction method and DPPH radical scavenging activity (%) at 10 μg/ml and EC50 (μg/ml) obtained from BHA.

Table 2

DPPH radical scavenging activity (%) at 1 mg/ml and EC50 (mg/ml) of lipid classes obtained from chloroform/methanol and supercritical carbon dioxide extraction from Sargassum muticum according to the extraction method and DPPH radical scavenging activity (%) at 10 μg/ml and EC50 (μg/ml) obtained from BHA.

4 Conclusion

It can be concluded that supercritical carbon dioxide can be used to extract antioxidant lipids from S. chordalis and S. muticum. The results indicated that each of the lipid fractions, i.e., neutral lipids, glycolipids and phospholipids, exhibited free radical scavenging compounds. The findings of this work demonstrated that non-polar lipids are the most active fraction when they are extracted with solvent mixture and polar lipids either glycolipids or phospholipids are the most active lipid class when the extraction was conducted with supercritical carbon dioxide. This work is useful to partially validate the bio-refinery approach and to up-grade the seaweed regarding antioxidant compounds in the cosmetic field.

Conflicts of interest

The authors declare that they have no conflict of interest in relation to this article.

Acknowledgements

The authors thank the PhD students Marie Lang and Maya Puspita from South Brittany University for collecting the seaweeds. This work is a part of research conducted by a temporary lecturer position at South Brittany University and at the LBCM laboratory.

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Cite this article as: Terme N, Boulho R, Kucma J-P, Bourgougnon N, Bedoux G. 2018. Radical scavenging activity of lipids from seaweeds isolated by solid-liquid extraction and supercritical fluids. OCL 25(5): D505.

All Tables

Table 1

DPPH radical scavenging activity (%) at 1 mg/ml and EC50 (mg/ml) of the lipid classes obtained from Solieria chordalis according to the extraction method and DPPH radical scavenging activity (%) at 10 μg/ml and EC50 (μg/ml) obtained from BHA.

Table 2

DPPH radical scavenging activity (%) at 1 mg/ml and EC50 (mg/ml) of lipid classes obtained from chloroform/methanol and supercritical carbon dioxide extraction from Sargassum muticum according to the extraction method and DPPH radical scavenging activity (%) at 10 μg/ml and EC50 (μg/ml) obtained from BHA.

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