Next Article in Journal
Factors Underlying Food Choice Motives in a Brazilian Sample: The Association with Socioeconomic Factors and Risk Perceptions about Chronic Diseases
Next Article in Special Issue
Metal Chelates of Petunidin Derivatives Exhibit Enhanced Color and Stability
Previous Article in Journal
Fungi Burger from Stale Bread? A Case Study on Perceptions of a Novel Protein-Rich Food Product Made from an Edible Fungus
Previous Article in Special Issue
Black Bean Anthocyanin-Rich Extract from Supercritical and Pressurized Extraction Increased In Vitro Antidiabetic Potential, While Having Similar Storage Stability
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Foods
Volume 9
Issue 8
10.3390/foods9081113
foods-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Scientific Approaches on Extraction, Purification and Stability for the Commercialization of Fucoxanthin Recovered from Brown Algae

by
Catarina Lourenço-Lopes
1,
Paula Garcia-Oliveira
1,2,
Maria Carpena
1,
Maria Fraga-Corral
1,2,
Cecilia Jimenez-Lopez
1,2,
Antia G. Pereira
1,2,
Miguel A. Prieto
1,2,* and
Jesus Simal-Gandara
1,*
1
Nutrition and Bromatology Group, Analytical and Food Chemistry Department, Faculty of Food Science and Technology, University of Vigo, Ourense Campus, E-32004 Ourense, Spain
2
Centro de Investigação de Montanha (CIMO), Instituto Politécnico de Bragança, Campus de Santa Apolonia, 5300-253 Bragança, Portugal
*
Authors to whom correspondence should be addressed.
Foods 2020, 9(8), 1113; https://doi.org/10.3390/foods9081113
Submission received: 9 July 2020 / Revised: 5 August 2020 / Accepted: 7 August 2020 / Published: 13 August 2020
(This article belongs to the Special Issue Chemical Characterization and Evaluation of Natural Pigments as Food Colorants)
Browse Figures
Versions Notes

Abstract

:
The scientific community has corroborated the numerous beneficial activities of fucoxanthin, such as its antioxidant, anti-inflammatory, anticancer or neuroprotective effects, among others. These properties have attracted the attention of nutraceutical, cosmetic and pharmacological industries, giving rise to various possible applications. Fucoxanthin may be chemically produced, but the extraction from natural sources is considered more cost-effective, efficient and eco-friendly. Thus, identifying suitable sources of this compound and giving a general overview of efficient extraction, quantification, purification and stabilization studies is of great importance for the future production and commercialization of fucoxanthin. The scientific research showed that most of the studies are performed using conventional techniques, but non-conventional techniques begin to gain popularity in the recovery of this compound. High Performance Liquid Chromatography (HPLC), Nuclear Magnetic Resonance (NMR) and spectroscopy techniques have been employed in the quantification and identification of fucoxanthin. The further purification of extracts has been mainly accomplished using purification columns. Finally, the stability of fucoxanthin has been assessed as a free molecule, in an emulsion, or encapsulated to identify the variables that might affect its further industrial application.

Graphical Abstract

1. Introduction

Traditionally, marine resources like micro- and macroalgae have been used as foods and medicines, mainly in oriental countries, such as China, Japan or Indonesia. However, their popularity is growing in western countries. In previous years, numerous studies have reported that these organisms present high nutritional values as foods and could be a possible source of compounds with bioactive potential. Several examples are fatty acids, carotenoids, polysaccharides, phytosterols, and phenolic compounds, which have been demonstrated to exert beneficial health effects, such as anticoagulant, antitumor or antioxidant properties [1]. Thus, the development of new formulations in food, cosmetic and pharmaceutical sectors using an algae compound is gaining relevance. Among macroalgae, brown ones (Class Phaeophyta) have been reported to present a greater amount of bioactive compounds, compared with red (Class Rhodophyta) and green (Class Chlorophyta) macroalgae [2]. Some bioactive compounds of brown macroalgae stand out such as phlorotannins, phylopheophylin and specially fucoxanthin [3]. Fucoxanthin is a secondary metabolite that belongs to the family of carotenoids and is present in the chloroplasts of algae cells. It is considered one of the most abundant and representative pigments of brown algae. This compound has been studied in numerous brown algae, such as in the genera Undaria, Sargassum, Laminaria, Eisenia, Alaria, Cystoseira or Hijikia [4,5], but it has also been found in red, green and unicellular microalgae [6,7,8].
Numerous scientific works have corroborated the beneficial activities of fucoxanthin, including antioxidant, anticancer, antihypertensive, anti-inflammatory, anti-diabetic, anti-obesity, neuroprotective, anti-angiogenic capacities and also photoprotective effects [4,7,9,10,11,12,13,14,15,16]. Considering these properties, the fucoxanthin molecule has a potential application in several industrial sectors such as food, cosmetic and pharmaceutical sectors. In fact, an expansion of the fucoxanthin market that might reach $120 million by 2022 is expected [17]. Nevertheless, the commercialization and production of this compound still have to face certain challenges, since its chemical synthesis is a complex and inefficient process, and the method of extraction from marine organisms has not been yet standardized [18,19]. To achieve the profitably of a product, it should be easily and quickly obtained, using low-cost technologies [20]. Although fucoxanthin and other carotenoids may be artificially synthesized, their extraction from natural sources presents several advantages, such as easy accessibility to the sources and an economic and environmentally friendly production, avoiding the use of dangerous chemical compounds. Consequently, future and innovative studies about extraction methods would be of great interest to favor the commercialization of fucoxanthin.
Several studies have cultivated brown algae to extract fucoxanthin, and many aspects have been demonstrated to influence its content, including environmental factors (water temperature, composition, light, etc.), stage of the life cycle or seasonal variations. Undaria pinnatifida is recognized as a key species to produce fucoxanthin and has been widely cultured in oriental countries (mostly in Japan, Korea and China), but its culture is growing in western ones. This species has been cultivated in deep seawater, due to several advantages, like the abundance of nutrients and low presence of pathogens. In this situation, the fucoxanthin content ranged between 0.32–2.67 mg/g, being lower in the later stages than in the younger stages of the life cycle [21]. In another study, U. pinnatifida was collected from two localizations during the growing season. The variations in the fucoxanthin content between localizations were attributed to environmental factors, such as sunlight, temperature and the amount of nutrients present in the water. In both locations, the content peaked between winter and spring, while the lowest peak was detected in summer. In addition, the blade of the algae (structure used for food applications) showed a higher fucoxanthin content, compared with sporophyll (reproductive structure, not consumed) [22]. Similar spatial and seasonal variations have been observed in other brown algae species such as Sargassum horneri, Cystoseira hakodatensis and Nizamuddinia zanardinii [23,24,25].
Considering all the factors that influence the fucoxanthin content, the obtaining process should be optimized to obtain the highest wield possible. The present study aims to provide a full vision of extraction, quantification, and purification methods that will allow the choice of the optimal protocol for recovering the highest ratio of fucoxanthin depending on the selected species and the laboratory facilities available. Also, three stabilization methods of the molecule will be reviewed, due to the importance of preventing fucoxanthin losses induced by degradation reactions. A general overview is presented in Figure 1.

2. Extraction Methods

Scientific literature shows several fucoxanthin extraction techniques employed to improve the extraction yields and to reduce costs. In this section, the methods will be presented in terms of yield. Table 1 compiles an extended list of brown algae in which fucoxanthin has been extracted using conventional and non-conventional techniques, respectively. In addition, the detection methods and their concentrations are also mentioned.

2.1. Conventional Techniques

2.1.1. Maceration Extraction (ME)

Most of the developed techniques found throughout the literature for obtaining fucoxanthin are based on ME protocols, which have been historically used for common extraction processes. This technique consists of a solid/liquid extraction in which different variables are evaluated, such as biomass-solvent ratio, percentage of solvent, time and temperature of incubation [26]. The biomass: solvent ratio used for optimizing the protocols has been observed to vary a lot with wide ranges going from 1:10 up to 1:500 [27,28]. Temperature and time of extraction are also very variable. The controlled temperatures tested for ME ranged from 4 °C up to 65 °C or in ice baths or at room temperatures, while evaluated times have ranged from 15 min up to 96 h. Besides, when extracting fucoxanthin, the choice of solvent is very important since it determines the efficiency of the extraction process. Among the examples provided, the most utilized solvents have been methanol (MeOH), acetone (AcO) and ethanol (EtOH), which have been applied at different percentages. Other studies have been performed using alternative options such as water (W), hexane (Hx), chloroform (Ch), dichloromethane (DCM), heptane (Hp) or diethyl ether (DE). According to some investigations, the preferred solvent was EtOH [28,29]. However, in a two-level full factorial design for the extraction of fucoxanthin from S. siliquosum and S. polycystum, the best solvent was MeOH. In this study, the optimized parameters were temperature (4–45 °C), time (30–1440 min), and solvent to solid ratio (10–50 mL/g), with extraction time. The best conditions were achieved at 30 min and a 45 °C of temperature with a low solvent to solid ratio of 5 mL/g. Fucoxanthin content obtained for S. siliquosum and S. polycystum was 491.47 and 449.90 µg/g dry weight (DW) when using EtOH and 706.98 and 521.34 µg/g DW for MeOH, respectively [30]. Similarly, the effect of incubation time, temperature, pH, and percentage of solvent was analyzed in a study based on nine different brown algae species [31]. The optimization determined that the yield was maxim at 30 °C for 36.5 min, pH5.7, using 62.2% AcO. In this study, the efficiency of conventional extraction methods was limited by the presence of branched, sulfated or complex polysaccharides (alginate, laminarin, etc.) in algal cell walls [31].

2.1.2. Vortex Assisted Extraction (VAE)

Recently, a study conducted with several brown macroalgae used and validated a VAE system, based on the traditional solid/liquid extraction, whose efficiency is improved by stirring. The results showed that the optimal yield was achieved by using 25 mg of the sample with 300 μL of EtOH and vortexed for 15 min [32].

2.1.3. Soxhlet Assisted Extraction (SAE)

This system is a dynamic process based on continuous reflux of solvent, generally used for health, food and environmental analysis. Temperature is a key factor when it comes to extraction, thus its increase is related to a better extraction since it can break interactions among molecules and facilitate the extraction [33]. SAE with heat application offers an alternative for ME with lower solvent consumption as it allows recircularization. A recent study showed an extraction yield of 0.45 mg/g for the macroalgae Saccharina japonica, using n-hexane (n-Hx) as solvent at 40 °C for 16 h [34]. Another study with Undaria pinnatifida displayed that the best conditions in SAE were 12 h at 78 °C with EtOH resulting in a yield of 50 µg/g [19].

2.2. Non-Conventional Techniques

On the other hand, advances in green technologies currently offer a wide spectrum of solid/liquid procedures that are quite useful for the extraction of the compounds of interest. Some of these emerging technologies involve microwave-assisted extraction, supercritical fluid extraction or ultrasound-assisted extraction, among others. All these methods can be referred to as non-conventional extraction techniques.

2.2.1. Enzyme-Assisted Extraction (EAE)

The main advantage of this method is the ability of enzymes to break the cellulose (hydrolysis) walls of the algae, favoring the accessibility to pigments. Moreover, it is a green technology with no toxic waste and is relatively cheap regarding the cost-effectiveness of the enzymes. A study with Fucus vesiculosus shows that by using the enzyme Viscozyme, the best conditions were enzyme-to-W ratio 0.52%, seaweed-to-W ratio 5.37% and enzyme incubation time 3 h. These conditions allowed 0.657 mg/g DW of fucoxanthin to be obtained [35]. Almost a complete recovery of fucoxanthin (96%) extraction was achieved through U. pinnatifida by using an enzymatic pre-treatment and then dimethyl ether (DME)+EtOH. The optimum parameters for the pre-treatment were 37 °C at pH6.2 for 2 h, 5% (w/v) solids, with 0.05% weight enzyme using continuous mixing [36].

2.2.2. Microwave-Assisted Extraction (MAE)

This technique has proved to be suitable for the extraction of bioactive compounds from algae as a viable alternative. A study employed MAE to extract fucoxanthin from L. japonica, U. pinnatifida, and S. fusiforme, using different solvents. Among them, EtOH and Ac obtained the best yields. For safety reasons, EtOH was chosen for further analysis. The extraction conditions were solvent to sample ratio of 10:1 (mL/g) at 50 °C for 10 min. The yields obtained were 5.13, 109.30, and 2.12 mg/100 g, for each algae, respectively [37]. The patent with reference CN104327017A claims a microwave-assisted extraction using EtOH as a solvent in only 5 min, being able to easily perform large-scale production. Then, a liquid-liquid extraction and column chromatography two-step separation process are applied to effectively separate fucoxanthin from chlorophyll and other impurity components.

2.2.3. Ultrasound-Assisted Extraction (UEA)

This technique is considered to be cost-effective and efficient, which utilizes ultrasounds to create micro-bubbles inside the solvent. The growth and collapse of the bubbles cause the breakdown of the macroalgae cell wall, favoring the penetration of the solvent. This technique has been employed to extract fucoxanthin from Padina tetrastromatica. The optimized values for solvent concentration, temperature and time were EtOH 80%, 50 °C, and 30 min, respectively. These conditions allowed 750 µg/g DW of fucoxanthin to be obtained, which was higher than the fucoxanthin content obtained with conventional extraction [20].

2.2.4. Pressurized Liquid Extraction (PLE)

This technique is based on applying high temperatures and pressures using a liquid solvent. It is also a green method, as it uses low quantities of solvent and short times. A study performed with the brown algae Eisenia bicyclis was done with this technique. It was observed that the parameters that influenced it were temperature and EtOH concentration, with 110 °C and 90% EtOH as the optimal values, obtaining a yield of 0.42 mg/g [38].

2.2.5. Supercritical Fluid Extraction (SFE)

This type of non-conventional extraction requires the fluid to reach a temperature and pressure above the critical point. Among its advantages, some of them can be highlighted as it has great extraction selectivity, short processing times, requires minimal solvents and a low degradability of the extracted product. The most used solvent is carbon dioxide (CO2) due to its thermodynamics and heat transfer properties. Moreover, it has a low critical point (31 °C, 73 bar). A co-solvent can be used to modify the extractant polarity. The most important parameters are temperature, pressure and co-solvent [39]. SFE has been applied to U. pinnatifida, using EtOH as co-solvent and different ranges of temperature (from 30–60 °C) and pressure (from 80–300 bar) were tested. Higher temperatures (50 °C) and pressures (200 bar) provided a value of 7.53 ng/g DW [40]. Another study based on U. pinnatifida showed that the two best conditions for SFE were, for the approach without entrainer, 70 °C and 400 bars for 3 h, which allowed a fucoxanthin yield of 60.12 µg/g to be obtained. The most efficient extraction method required the use of EtOH as entrainer for very similar conditions (60 °C and 400 bar for 3 h) and allowed a fucoxanthin yield of 994.53 µg/g to be achieved [19]. The functionality of this technique also allowed extracting rich-fucoxanthin oil fractions from two brown seaweeds, S. japonica, and S. horneri. The optimized conditions consisted of a flow rate of 27 mg/min of CO2 at a temperature of 45 °C and a pressure of 250 bar for 2 h. Under these parameters, the concentration of fucoxanthin was 0.41 ± 0.05 mg/g for S. japonica and 0.77 ± 0.07 mg/g for S. horneri. The SFE extracts showed greater in vitro activity than the extracts obtained with other techniques [41].

2.3. Comparison of Extraction Systems

The main objective of the comparison is to elucidate the most efficient extraction methods in terms of recovery. As observed in Table 1, a great variability among brown macroalgae extracted, different solvents, and different extraction conditions exist. Taking this into account, it is very complex to perform a comparison. When possible, studies using the same species, but different extraction systems were selected and further discussed in this section. U. pinnatifida has been the most studied macroalgae species and has been extracted using different techniques: MAE, PLE, SFE, and ME. The highest values reported were 2.671 mg/g DW and 4.96 mg/g fresh weight (FW) using ME [21,22]. Laminaria japonica and S. fusiforme have been extracted by ME and MAE. As in the previous case, the conventional ME allowed a greater content to be obtained (0.19 and 6.62 mg/g DW for L. japonica and S. fusiforme, respectively) compared to MAE (0.04 and 0.06 mg/g DW, respectively) [37,42,43]. CE and SFE systems have been utilized with the macroalgae species F. serratus and S. horneri. For F. serratus, the studies reported quite similar fucoxanthin content, 3.57 and 2.18 mg/g DW for ME and SFE, respectively. Regarding S. horneri, yield differences were more pronounced, obtaining 4.49 and 0.77 mg/g DW of fucoxanthin using ME and SFE, respectively [27]. F. vesiculosus has been extracted by VAE and EAE, both techniques showing similar fucoxanthin recovery values: 0.70 and 0.66 mg/g DW, respectively [31,35]. Several studies have extracted fucoxanthin from Dictyota dichotoma using ME and VAE. In this case, the differences in the extraction yield were noticeable, since ME extracted 6.42 mg/g DW of fucoxanthin, versus 0.60 mg/g DW obtained with VAE. Finally, P. tetrastromatica has been extracted by using ME and UAE. Both techniques extracted a similar content of fucoxanthin, specifically, 0.41 and 0.75 mg/g DW [20,44].
Concluding, the ME has been used in a great variety of brown algae and, in general, is the best technique in terms of fucoxanthin recovery. Conventional techniques are low cost and present lower performance difficulty [45]. However, in several cases, the extraction times are long (which may cause deterioration of fucoxanthin) and the solvents used are toxics, such as MeOH. Compared to ME, few studies have been performed using the non-conventional techniques mentioned in this study. According to the scientific literature performed, SFE might be the best non-conventional technique, in terms of extraction efficiency. One of the advantages of this system is the use of CO2 as a solvent, an easy-available compound and non-toxic. Although more studies are still needed, SFE systems could be an efficient and respectful option for the industrial production of fucoxanthin.

3. Quantification, Identification, and Purification Methods

3.1. Quantification and Identification of Fucoxanthin

Fucoxanthin is a pigment that offers different alternatives for its quantification since it can be performed through analytical techniques (based on its molecular mass detection), spectrophotometric methods (based on its color feature), or a combination of both systems. The most common instruments utilized for its identification and quantification are: (1) liquid chromatography-mass spectrometry (LC-MS) using mass-to-charge ratio (m/z); (2) high-performance liquid chromatography (HPLC) coupled to ultraviolet (UV) or (photo)diode array detectors (PDA/DAD), which detects maximum absorbance peak at 446 nm; (3) nuclear magnetic resonance (NMR), which determines its structure; or (4) spectrophotometric readers that provide absorbance based data [28]. Most of the protocols developed for the quantification of fucoxanthin using LC, either HPLC or UPLC equipment, usually establish absorbance around 450 nm. For instance, samples from Turbinaria turbinata and S. plagyophyllum were analyzed selecting a detection wavelength of 450 nm [56]. However, the presence of conjugated double bonds in the fucoxanthin formula (Figure 1) make it unstable under some conditions. Fucoxanthin can get isomerized into cis-fucoxanthin, whose oxidation may produce short-chain carbonyl compounds. To detect and provide an accurate fucoxanthin quantification, it is useful to perform wide spectra readings (from 300 to 500 nm) or establish the specific wavelengths associated with these sub-products (300, 350 and 400 nm) [60]. Regarding LC-MS, the quantification of the fucoxanthin has been mostly performed by LC-MS, using either electrospray or atmospheric pressure chemical ionization (ESI or APCI, respectively) sources and coupled to additional detectors such as UV or DAD, among others [37,52,60,61,62]. Other approaches include different mass detector improvements, like UPLC-PDA-TWIMS-QTOF-MS (UPLC-PDA coupled to a quadrupole/traveling-wave ion mobility/time-of-flight MS) [63]. Among the spectrometric techniques used for identifying fucoxanthin, Fourier transform infrared (FTIR) has been used in the region of 500 to 4000 cm−1 for characterizing purified fractions obtained from extracts of Himanthalia elongata. In the same study, an UV-visible detector coupled to DAD (190 to 600 nm) also provided spectroscopy results [64]. NMR techniques are very useful tools for the identification and the structural determination of fucoxanthin and its sub-products. In fact, it has been used as a confirmatory instrument in many fucoxanthin-related works [4,21,37,52,61,65,66,67,68]. Finally, spectrophotometry techniques have been widely utilized for the identification and quantification of several pigments, mostly as a sum of carotenoids. To obtain robust data, spectrophotometric methods require the previous adjustment of the quantification protocol to the specific experimental conditions: establish the correct titration of the sample, adapt reading parameters and equations to different solvents, and determine adequate negative and positive controls [44,69,70]. The specific quantification of fucoxanthin by spectrophotometry has been scarcely developed [44,71]. Nevertheless, they have been described as easier, faster and cheaper than LC. A study analyzed the content of fucoxanthin extracts using a microplate reader. This technique allowed results with lower standard errors (<5%) than HPLC to be obtained [71]. Spectrophotometric methods are cheaper since they reduce experimental times, do not require highly trained personnel or equipment for their development, nor do they use a high volume of organic solvents, so they can be also considered as greener techniques than those that are LC-based. The preferred quantification method for fucoxanthin still remains to be those based on the use of HPLC or LC instruments; however cheaper, quicker, and easier options like spectrophotometry have been suggested as a promising screening tool.

3.2. Purification

Fucoxanthin-rich extracts may be concentrated and further purified. For the performance of this step, extracts can be loaded onto a silica gel packed into a glass column and with a solvent. The solvent type varies throughout scientific literature; however, n-Hx is frequently used as part of a mixture of solvents, for example, n-Hx:AcO, which has been applied in different proportions such as 6:4 (v:v) and 7:3 (v:v) [28,72]. Another study used a few solvents starting with a mixture of n-Hx:DE that gradually reduced the amount of n-Hx from 80 up to 0, then finished with MeOH. This option showed a co-elution of lipids. Thus, to achieve a higher degree of purity, fractions were dissolved in Ch and applied on preparative thin-layer chromatography plates using a combination of Hx/De/acetic acid (70:30:1, volume-based) and MeOH. To separate neutral lipids, the latter solution may be used, and for the polar ones, Ch/AcO/MeOH/acetic acid/W (50:20:10:10:5, volume-based) [63]. Similarly, another work used Ch/DE/n-Hx/acetic acid (10:3:1:1, volume-based) to obtain a purified extract of fucoxanthin [64]. Another method of purification is based on salt aqueous two-phase systems, but this process needs additional purification steps. An effective alternative is the use of ultra-filtration to process an ethanolic salt aqueous two-phase system which may reduce the unspecific losses of the pigment as well as the amount of protein impurities, allowing an increase in the purity of the permeate up to 63% [73]. After the selected purification step, the orange-red fraction that contains fucoxanthin is collected and can be submitted to further purification stages with a process like prep-HPLC. After its separation, the fraction of interest is further analyzed to identify it.

4. Molecule Stability

Once fucoxanthin has been extracted, it is fundamental to store it under stable conditions, paying special attention to its exposure to light, extreme pH value or temperature. This section offers an overview of the stability studies performed with fucoxanthin. Three different approaches, which are presented below in increasing order of complexity, have been developed to confirm the chemical stability of the molecule. The evaluation of fucoxanthin has been performed of the free compound, embedded as part of an emulsion, or encapsulated.

4.1. Free Molecule

The unique chemical characteristics of fucoxanthin (unusual allenic bond, epoxide group, and conjugated carbonyl group within a polyene chain) (Figure 1) confer several oxidation targets to this molecule. The main factors that can trigger carotenoids degradation are oxygen, light, high temperatures, enzymatic reactions, heavy metals exposure, and extended periods of storage [74,75,76,77,78,79]. Different studies have evaluated the stability of fucoxanthin in terms of temperature when freely added to diverse matrixes. The stability of free fucoxanthin in water and milk was observed to decrease with the increment of the temperature. At 2 °C, fucoxanthin was stable for 28 days in milk. After 28 days at 10 and 26 °C, fucoxanthin stability in milk was reduced by about 20%. In water, the compound showed a degradation of nearly 40 and 80%, at 10 and 26 °C, respectively [80]. However, other experiments showed no significant differences in rich-fucoxanthin extracts stored at 4 °C or 25 °C (p > 0.05) for 4 weeks. The treatment at 50 °C temperature displayed a significant decrease in the stability of the fucoxanthin after the third week of storage [65]. Similar results were obtained when fucoxanthin was subdued to 75 °C for 60 min, showing a stability loss of 94%. At 25 °C, this level of stability loss is reached between the fourth (87%) and the ninth (99%) day [74]. Other works have evaluated fucoxanthin stability in terms of pH. A stability study analyzed extracts obtained from S. binderi treated at different pH conditions. The initial pH (6.1) of the fucoxanthin-rich extract was shifted to both very acidic (pH of 1 and 3) and very alkaline (pH of 9, 11 and 13) environments. It was found that the ideal range to extend fucoxanthin stability is in a pH between 5 and 7 [65]. The chemical behavior of free fucoxanthin was also evaluated under a digestibility in vitro model where the samples were exposed to different molecules and pH changes (from 2.2 to 7.0). The results showed a progressive degradation from the simulated stomach conditions (10%) to the ileum (20%) accompanied by a transformation into fucoxanthinol. This metabolite represented more than 50% of the fucoxanthin in the duodenum and nearly 100% in the ileum [75]. Finally, light has been also considered in the stability determination. Fucoxanthin is a pigment that has been demonstrated to be sensitive to light exposure. When free fucoxanthin is preserved at darkness the molecule is more stable than when exposed to light. Under light the stability drops more than 50% after 4 days of storage [65]. Other work that utilized longer storage periods confirmed that keeping fucoxanthin in darkness extended its shelf-life with a degradation rate lower than 10% [81]. Therefore, the optimal storage conditions for free fucoxanthin include its conservation in darkness, in a solution with a pH between 5 and 7, and at low temperatures, preferably those lower than room temperature.

4.2. In Emulsions

The inclusion of ingredients in emulsions is usually considered a good option to achieve the stabilization of the compound. Food grade emulsions consist of creating small lipid droplets dispersed in water that may be utilized for incorporating different molecules of interest into fatty food matrixes. The inclusion of the biomolecules into the droplets improves their bioavailability since it preserves their bioactivities and their chemical features. A study studied the fucoxanthin stability when incorporated into oil-in-water emulsions using different natural emulsifiers (whey protein isolate, lecithin and Arabic gum). Among the tested emulsifiers, whey protein was the one that provided better stability to fucoxanthin. This emulsifier slowed down the degradation of fucoxanthin, displaying a 30% loss after 15 days of storage at 25 °C while Arabic gum and lecithin emulsions showed a 60% degradation in the first five days [82]. In another study, fucoxanthin was loaded into emulsions using carrier oils with different properties: oils with long and medium-chain triacylglycerols and indigestible oils. This study concluded that fucoxanthin was more soluble and got absorbed better when included into micelles created with oils containing long and medium-chain triacylglycerols. However, any of the tested emulsions provide similar fucoxanthin concentrations (being fucoxanthinol and amarouciaxanthin A quantified as fucoxanthin equivalents) when estimated in serum samples [83]. Finally, other research performed a further analysis of fucoxanthin after its emulsification in an oil/water system. It showed that total fucoxanthin and all its trans-, 13-cis and 13’-cis isomers suffered a significant degradation when stored at different temperatures. The stability decrease was stronger when fucoxanthin-like molecules were subdued to 60 °C, since the nearly total loss was detected after the fifth day of storage. This degradation rate was slower when applying temperatures of 5 °C and 37 °C showing 80% losses after 40 of 14 storage days, respectively. Total and all-trans fucoxanthin suffered degradation with temperature dependence and promoted the formation of complexes of activated structures, which are more sensitive to degradation. When samples were exposed to light and pH was reduced, the degradation rates were much more dramatic but promoted the formation of the 9’-cis isomer. This compound was the only one that was able to resist these treatments in the emulsion, except at low values of pH. It increased its concentration under neutral pH of 7.5 or light exposition since the isomerization reaction predominated over the degradation one induced by oxidation, protonation or illumination. In actuality, the degradation rate of the 9’-cis isomer was lower than for fucoxanthin and its isomers (all-trans, 13-cis, and 13’-cis) in the emulsion. In this study, the stability of fucoxanthin-like molecules in emulsions was deeply analyzed, showing that the extrinsic factors determining their degradation were established from greater to lower influence: pH, temperature and exposure to light [84]. Therefore, further studies should be conducted to disclose the effect of different emulsifiers or carrier oils on the stability of fucoxanthin isomers. Nevertheless, their addition seems to be required to prolong the stability of fucoxanthin-like molecules when incorporated into emulsions.

4.3. Encapsulation

Encapsulation is a process that provides a physical barrier to prevent the alteration of the core ingredient. This technique stabilizes and protects molecules that get easily degraded, hence encapsulation allows the fortification of different matrixes with compounds that otherwise would have lost their bioactivities. The stability and bioavailability of fucoxanthin when encapsulated using different approaches and materials has been evaluated. The variability of wall materials that have been used for developing capsules is huge. Different proteins (whey, zein, casein and gelatin), oligosaccharides (maltodextrins, cyclodextrin), polysaccharides (chitosan, alginates) or glycolipids are commonly employed as encapsulation materials, applied both individually or combined. A study evaluated up to six ingredients to microencapsulate fucoxanthin: hydroxypropyl-β-cyclodextrin, maltodextrin, gum Arabic, whey protein isolate, isolated pea protein and gelatin. After exposing microcapsules to a temperature of 90 °C for 24 h, those built with whey protein isolate, gum Arabic, and maltodextrin displayed the lower degradation rates with values of 38%, 44% and 45%, respectively [76]. Another work utilized nanogels prepared by ionic gelation with different amounts of chitosan and glycolipid or sodium tripolyphosphate. The analysis performed with an FTIR revealed that fucoxanthin creates numerous hydrogen bonds with chitosan. Results obtained from X-ray tests showed that fucoxanthin gets arranged in a disorderly manner within the chitosan-nanogels. However, fucoxanthin remained more stable when introduced into nanogels formed by the combination of chitosan with glycolipid. The presence of glycolipid improves its stability, prolongs the storage time and avoids its degradation up to 45 h. Regarding the biological availability of fucoxanthin, an in vitro test demonstrated that the use of chitosan-glycolipid nanogels offered the highest bioavailability rate (68%), followed by chitosan (51%) and glycolipid nanogels (35.5%) [85]. Another work compared the efficiency of fucoxanthin encapsulated into casein nanoparticles and the same nanoparticles but with a chitosan coat. Both kinds of particles were submitted to a simulated digestion process in an in vitro assay where they were presented to different enzymes and fluid secretions (α-amylase, pepsin, bile extract, pancreatic lipase, and pancreatin) and pH changes (from 6.5 to 2.2, then to 5.5, slowly increased to 6.0 and 7.0). The pass of fucoxanthin through the gastrointestinal tract has been demonstrated to trigger its transformation into fucoxanthinol. Fucoxanthin contained into the nanoparticles also get transformed into fucoxanthinol. However, those additionally coated with chitosan slowed down the process and also provided slight degradation rates (20%) that were mostly observed during the steps simulating the jejunum and ileum [75]. Another approach also based on the use of casein (sodium caseinate) showed the advantages of mixing it with zein to create nanoparticles (100 to 130 nm). Both components of the nanocapsules interacted with fucoxanthin by hydrophobic contacts, which seemed to stabilize the molecule and its bioactivities since after heating fucoxanthin (75 °C) it remained stable for 60 min, showing an estimated 20% degradation after 140 min. Other nanoparticles created with just caseinate or just zein showed about 15% and 30% degradation rate after 60 min, respectively. The caseinate-zein nanocapsules also extend the stability of fucoxanthin when stored at 25 °C for further than 16 days showing at that time a degradation rate lower than 30% [74]. Therefore, encapsulation allows the isolation of the target ingredients, providing chemical stability, which ultimately will preserve their bioactivities, and also allows the determination of an exact dosage. The incorporation of exact concentrations into a matrix may represent a comfortable administration format to the consumers, which will allow the maximization of health benefits associated with fucoxanthin which are mostly dose-dependent. Hence, the encapsulation of fucoxanthin is an accurate method to specify its final amount, facilitating the potential adherence for fucoxanthin-based treatments [86].

5. Developed Products Containing Fucoxanthin and Their Health Benefits

The optimization of the extractive process, purification and stabilization of this molecule is of great interest to the industry due to the several therapeutic activities described, making it a useful compound to incorporate in nutraceuticals, cosmetics, and even pharmaceutical products. As mentioned before, fucoxanthin has gathered much attention of late due to its strong antioxidant proprieties, anti-cancer, anti-inflammatory activities and anti-obesity effects, among others (Figure 2) [87]. Regarding the last property, fucoxanthin can be added as a food component to accelerate the adaptive thermogenesis [88]. U. pinnatifida lipids, containing 9.6% fucoxanthin, significantly reduced the weight of abdominal white adipose tissue of rats and mice. Bodyweight of mice fed with 2% of Undaria lipids was significantly lower than that of controls [89]. These results suggest that fucoxanthin could be used in dietary supplements with anti-obesity potential, to treat or prevent diseases related to excessive weight. Currently, these supplements can be found in the market, in the form of oil or as a microencapsulated powder with the commercial name of ThinOgen® and Fucovital®, for example. They are supposed to help weight loss and also improve eye, brain, liver, and joint health [90]. Furthermore, fucoxanthin may be used to combat neurodegeneration. The neuroprotective proprieties of this molecule were tested in models of traumatic brain injury. In vitro studies demonstrated that fucoxanthin increased neuron survival and reduced the reactive oxygen species levels [91]. It was observed that the administration of fucoxanthin in cerebral ischemic/reperfusion injury models suggested that this pigment could be exploited as a therapeutic target for protecting neurons [92]. These results point out that the use of fucoxanthin as a nutritional supplement could be interesting for the prevention or even the treatment of brain injuries and neurodegenerative pathologies. Some studies conducted about this are already incorporating fucoxanthin in several foods, such as enriched canola oil [93], fortified yogurt [94], milk [95], baked products like scones [96] and even ground chicken breast meat [97].
In the cosmetics and pharmaceutical industries, this carotenoid is also relevant, due to its skin protective effects against burns and filaggrin (filament aggregating protein) disorder induced by radiation. Fucoxanthin demonstrated great results against UV radiation and was able to protect the dermal layers. This dermoprotective capacity can be explained through the promotion of filaggrin which generates a dermal barrier [98]. This protection has also been associated with the remediation of DNA damage and the potent antioxidant activity of fucoxanthin in human fibroblast cells [99]. An inhibitory effect on tyrosinase activity in guinea pigs exposed to UV radiation was also reported, showing a decrease in the harmful effects. Other study demonstrated that oral administration of fucoxanthin produced a suppression of the transcription of the melanogenesis factor, due to the inhibition of dermal mRNA expression related to this disease [100]. These results seem to indicate that the oral or topical administration of fucoxanthin can prevent or even reduce the negative effects induced by UV radiation exposure, such as the appearance of melanomas. In fact, due to its antioxidant capacity, fucoxanthin has been tested in several anti-aging and anti-sun cosmetic formulations [101,102].

6. Future Perspectives and Conclusions

Fucoxanthin is considered a valuable molecule due to its wide range of beneficial properties, like antioxidant activity, cardiovascular protection, neuroprotective effect or photoprotective properties, among others. All these turn fucoxanthin into an interesting pigment with promising industrial applications in the food, cosmetic and pharmaceutical sectors. Nevertheless, the commercialization of fucoxanthin is scarce, which greatly limits its further use. As mentioned before, fucoxanthin may be chemically synthesized, but this process is inefficient and complex, while the extraction method from marine organisms has not been standardized. Therefore, it is necessary to design a practical way to profit from its properties. First would be the extraction of fucoxanthin from brown macroalgae, as there is easy and economic access to these organisms, and it avoids the safety issues prompted using chemical compounds. However, the extraction yield of fucoxanthin has been found to be very variable depending on the selected species and the recovery technique, as demonstrated by the data provided from the analyzed scientific literature. In this context, further studies are needed to standardize the fucoxanthin obtaining process. The application of methods like response surface methodology is likely to optimize extraction conditions for fucoxanthin. Moreover, even though conventional techniques are widely employed, non-conventional extraction techniques are gaining importance and new approaches are expected. Once fucoxanthin has been extracted, it is fundamental to store it under stable conditions, paying special attention to its exposure to light, extreme pH values, or temperatures. The encapsulation of fucoxanthin has been revealed to be the most profitable technique for the conservation of fucoxanthin-like molecules. Nowadays, different products have been fortified with fucoxanthin and proved to exert different health benefits (such as loss weight loss or antioxidant capacity, among others).
In conclusion, the selection of the extraction and purification methods is a key factor to achieve acceptable yields, prevent pigment degradation and reduce production costs. In addition, the use of environmentally friendly extraction/purification techniques may increase the commercial value of the final product. Among the different extraction methods provided in this article, it is necessary to standardize the experimental conditions, especially when scaling up the process to an industrial level. Regarding the storage alternatives, fucoxanthin encapsulation using natural products is considered as one of the best approaches, followed by its emulsion using natural emulsifiers. Therefore, future and innovative studies regarding efficient, quick, eco-friendly and safe extraction methods can speed up the progress towards its commercialization and incorporation of fucoxanthin in the global market.

Author Contributions

Formal analysis, M.A.P. and J.S.-G.; Investigation, C.L.-L., P.G.-O., M.C., M.F.-C., C.J.-L., A.G.P., M.A.P. and J.S.-G.; Methodology, C.L.-L., P.G.-O., M.C., M.F.-C., C.J.-L. and A.G.P.; Supervision, M.A.P. and J.S.-G.; Validation, M.A.P. and J.S.-G.; Writing—original draft, C.L.-L., P.G.-O., M.C., M.F.-C., C.J.-L., A.G.P., M.A.P. and J.S.-G.; Writing—review and editing, M.A.P. and J.S.-G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by: Programa de Cooperación Interreg V-A España—Portugal (POCTEP) 2014–2020 (projects Ref.: 0181_NANOEATERS_01_E and Ref: 0377_IBERPHENOL_6_E); Axudas Conecta Peme (Xunta de Galicia, IN852A 2018/58 NeuroFood Project); Bio Based Industries Joint Undertaking (JU, No 888003 UP4HEALTH Project, H2020-BBI-JTI-2019); and Ibero-American Program on Science and Technology (CYTED-AQUA-CIBUS, P317RT0003).

Acknowledgments

The research leading to these results received financial support from Programa de Cooperación Interreg V-A España—Portugal (POCTEP) 2014–2020 (projects Ref.: 0181_NANOEATERS_01_E and Ref: 0377_IBERPHENOL_6_E) for supporting the pre-doctoral grant for C. Jimenez-Lopez; to MICINN supporting the Ramón&Cajal grant for M.A. Prieto (RYC-2017-22891); to Xunta de Galicia and University of Vigo supporting the post-doctoral grant for M. Fraga-Corral (ED481B-2019/096) and the pre-doctoral grants for A.G. Pereira (ED481A-2019/0228) and P. García-Oliveira (ED481A-2019/295); to Axudas Conecta Peme (Xunta de Galicia) supporting the IN852A 2018/58 NeuroFood Project and AlgaMar (www.algamar.com) for supporting the pre-doctoral grant for C. Lourenço-Lopes; to EcoChestnut Project (Erasmus+ KA202) for supporting the work of M. Carpena.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

Generic
DWDry weight
FWFresh weight
RTRoom temperature
Extraction techniques
EAEEnzyme-assisted extraction
MAEMicrowave-assisted extraction
MEMaceration extraction
PLEPressurized liquid extraction
SFESupercritical fluid extraction
VAEVortex assisted extraction
Compounds
AcOAcetone
ChChloroform
CO2Carbon dioxide
DCMDichloromethane
DEDiethyl ether
DMEDimethyl ether
EtOHEthanol
H2O2Hydrogen peroxide
HpHeptane
HxHexane
MeOHMethanol
n-Hxn-Hexane
WWater
Detection and purification techniques
13C-NMRCarbon-13 nuclear magnetic resonance
1H-NMRProton nuclear magnetic resonance
APCIAtmospheric Pressure Chemical Ionization
DADDiode-array detector
PDAPhotodiode-array detector
ESIElectrospray ionization
FTIRFourier-transform infrared spectroscopy
HPLCHigh-performance liquid chromatography
HPTLCHigh Performance Thin Layer Chromatography
LCLiquid chromatography
MSMass spectrometry
NMRNuclear Magnetic Resonance
QTOFQuadrupole time of flight
SpecSpectrophotometry
TWIMSTraveling-wave ion mobility MS
UPLCUltrahigh-performance liquid chromatography
UVUltraviolet

References

  1. Saet, B.L.; Joo, Y.L.; Song, D.G.; Pan, C.H.; Chu, W.N.; Min, C.K.; Eun, H.L.; Sang, H.J.; Kim, H.S.; Yeong, S.K.; et al. Cancer chemopreventive effects of Korean seaweed extracts. Food Sci. Biotechnol. 2008, 17, 613–622. [Google Scholar]
  2. Prabhasankar, P.; Ganesan, P.; Bhaskar, N.; Hirose, A.; Stephen, N.; Gowda, L.R.; Hosokawa, M.; Miyashita, K. Edible Japanese seaweed, wakame (Undaria pinnatifida) as an ingredient in pasta: Chemical, functional and structural evaluation. Food Chem. 2009, 115, 501–508. [Google Scholar] [CrossRef]
  3. Maeda, H.; Hosokawa, M.; Sashima, T.; Takahashi, N.; Kawada, T.; Miyashita, K. Fucoxanthin and its metabolite, fucoxanthinol, suppress adipocyte differentiation in 3T3-L1 cells. Int. J. Mol. Med. 2006, 18, 147–152. [Google Scholar] [CrossRef] [PubMed]
  4. Maoka, T.; Fujiwara, Y.; Hashimoto, K.; Akimoto, N. Characterization of fucoxanthin and fucoxanthinol esters in the Chinese surf clam, Mactra chinensis. J. Agric. Food Chem. 2007, 55, 1563–1567. [Google Scholar] [CrossRef] [PubMed]
  5. Willstatter, R.; Page, H. The pigments of the brown algae. Justus Liebigs Ann. Chem. 1914, 404, 237–271. [Google Scholar]
  6. Peng, J.; Yuan, J.P.; Wu, C.F.; Wang, J.H. Fucoxanthin, a marine carotenoid present in brown seaweeds and diatoms: Metabolism and bioactivities relevant to human health. Mar. Drugs 2011, 9, 1806–1828. [Google Scholar] [CrossRef] [PubMed]
  7. Mikami, K.; Hosokawa, M. Biosynthetic pathway and health benefits of fucoxanthin, an algae-specific xanthophyll in brown seaweeds. Int. J. Mol. Sci. 2013, 14, 13763–13781. [Google Scholar] [CrossRef] [Green Version]
  8. Palermo, J.A.; Gros, E.G.; Seldes, A.M. Carotenoids from three red algae of the Corallinaceae. Phytochemistry 1991, 30, 2983–2986. [Google Scholar] [CrossRef]
  9. Heo, S.J.; Ko, S.C.; Kang, S.M.; Kang, H.S.; Kim, J.P.; Kim, S.H.; Lee, K.W.; Cho, M.G.; Jeon, Y.J. Cytoprotective effect of fucoxanthin isolated from brown algae Sargassum siliquastrum against H2O2 -induced cell damage. Eur. Food Res. Technol. 2008, 228, 145–151. [Google Scholar] [CrossRef]
  10. Van Chuyen, H.; Eun, J.B. Marine carotenoids: Bioactivities and potential benefits to human health. Crit. Rev. Food Sci. Nutr. 2017, 57, 2600–2610. [Google Scholar] [CrossRef]
  11. Sugawara, T.; Yamashita, K.; Asai, A.; Nagao, A.; Shiraishi, T.; Imai, I.; Hirata, T. Esterification of xanthophylls by human intestinal Caco-2 cells. Arch. Biochem. Biophys. 2009, 483, 205–212. [Google Scholar] [CrossRef]
  12. Gómez-Zavaglia, A.; Prieto, M.A.; Jiménez-López, C.; Mejuto, J.C.; Simal-Gándara, J. The potential of seaweeds as a source of functional ingredients of prebiotic and antioxidant value. Antioxidants 2019, 8, 406. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. D’Orazio, N.; Gemello, E.; Gammone, M.A.; De Girolamo, M.; Ficoneri, C.; Riccioni, G. Fucoxantin: A treasure from the sea. Mar. Drugs 2012, 10, 604–616. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Kumar, S.R.; Hosokawa, M.; Miyashita, K. Fucoxanthin: A Marine Carotenoid Exerting Anti-Cancer Effects by Affecting Multiple Mechanisms. Mar. Drugs 2013, 11, 5130–5147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Kotake-Nara, E.; Yonekura, L.; Nagao, A. Lysoglyceroglycolipids improve the intestinal absorption of micellar fucoxanthin by Caco-2 cells. J. Oleo Sci. 2015, 64, 1207–1211. [Google Scholar] [CrossRef] [Green Version]
  16. Gao, K.; McKinley, K.R. Use of macroalgae for marine biomass production and CO2 remediation: A review. J. Appl. Phycol. 1994, 6, 45–60. [Google Scholar] [CrossRef]
  17. Research, I.M. Global Fucoxanthin Market Report 2018. 2018. Available online: https://www.businessindustryreports.com/report/102177/global-fucoxanthin-market-report-2018 (accessed on 5 July 2020).
  18. Yamamoto, K.; Ishikawa, C.; Katano, H.; Yasumoto, T.; Mori, N. Fucoxanthin and its deacetylated product, fucoxanthinol, induce apoptosis of primary effusion lymphomas. Cancer Lett. 2011, 300, 225–234. [Google Scholar] [CrossRef]
  19. Kanda, H.; Kamo, Y.; Machmudah, S.; Wahyudiono; Goto, M. Extraction of fucoxanthin from raw macroalgae excluding drying and cell wall disruption by liquefied dimethyl ether. Mar. Drugs 2014, 12, 2383–2396. [Google Scholar] [CrossRef]
  20. Raguraman, V.; MubarakAli, D.; Narendrakumar, G.; Thirugnanasambandam, R.; Kirubagaran, R.; Thajuddin, N. Unraveling rapid extraction of fucoxanthin from Padina tetrastromatica: Purification, characterization and biomedical application. Process Biochem. 2018, 73, 211–219. [Google Scholar] [CrossRef]
  21. Mori, K.; Ooi, T.; Hiraoka, M.; Oka, N.; Hamada, H.; Tamura, M.; Kusumi, T. Fucoxanthin and Its Metabolites in Edible Brown Algae Cultivated in Deep Seawater. Mar. Drugs 2004, 2, 63–72. [Google Scholar] [CrossRef] [Green Version]
  22. Fung, A.; Hamid, N.; Lu, J. Fucoxanthin content and antioxidant properties of Undaria pinnatifida. Food Chem. 2013, 136, 1055–1062. [Google Scholar] [CrossRef] [PubMed]
  23. Terasaki, M.; Kawagoe, C.; Ito, A.; Kumon, H.; Narayan, B.; Hosokawa, M.; Miyashita, K. Spatial and seasonal variations in the biofunctional lipid substances (fucoxanthin and fucosterol) of the laboratory-grown edible Japanese seaweed (Sargassum horneri Turner) cultured in the open sea. Saudi J. Biol. Sci. 2017, 24, 1475–1482. [Google Scholar] [CrossRef] [PubMed]
  24. Nomura, M.; Kamogawa, H.; Susanto, E.; Kawagoe, C.; Yasui, H.; Saga, N.; Hosokawa, M.; Miyashita, K. Seasonal variations of total lipids, fatty acid composition, and fucoxanthin contents of Sargassum horneri (Turner) and Cystoseira hakodatensis (Yendo) from the northern seashore of Japan. J. Appl. Phycol. 2013, 25, 1159–1169. [Google Scholar] [CrossRef]
  25. Fariman, G.A.; Shastan, S.J.; Zahedi, M.M. Seasonal variation of total lipid, fatty acids, fucoxanthin content, and antioxidant properties of two tropical brown algae (Nizamuddinia zanardinii and Cystoseira indica) from Iran. J. Appl. Phycol. 2016, 28, 1323–1331. [Google Scholar] [CrossRef]
  26. Pinela, J.; Prieto, M.A.; Pereira, E.; Jabeur, I.; Barreiro, M.F.; Barros, L.; Ferreira, I.C.F.R. Optimization of heat- and ultrasound-assisted extraction of anthocyanins from Hibiscus sabdariffa calyces for natural food colorants. Food Chem. 2019, 275, 309–321. [Google Scholar] [CrossRef] [Green Version]
  27. Heffernan, N.; Smyth, T.J.; FitzGerald, R.J.; Vila-Soler, A.; Mendiola, J.; Ibáñez, E.; Brunton, N.P. Comparison of extraction methods for selected carotenoids from macroalgae and the assessment of their seasonal/spatial variation. Innov. Food Sci. Emerg. Technol. 2016, 37, 221–228. [Google Scholar] [CrossRef] [Green Version]
  28. Xia, S.; Wang, K.; Wan, L.; Li, A.; Hu, Q.; Zhang, C. Production, characterization, and antioxidant activity of fucoxanthin from the marine diatom Odontella aurita. Mar. Drugs 2013, 11, 2667–2681. [Google Scholar] [CrossRef]
  29. Irvani, N.; Hajiaghaee, R.; Zarekarizi, A.R. A review on biosynthesis, health benefits and extraction methods of fucoxanthin, particular marine carotenoids in algae. J. Med. Plants 2018, 17, 6–30. [Google Scholar]
  30. Lim, M.W.S.; Tan, K.M.; Chew, L.Y.; Kong, K.W.; Yan, S.W. Application of Two-Level Full Factorial Design for the Extraction of Fucoxanthin and Antioxidant Activities from Sargassum siliquosum and Sargassum polycystum. J. Aquat. Food Prod. Technol. 2018, 27, 446–463. [Google Scholar] [CrossRef]
  31. Shannon, E.; Abu-Ghannam, N. Optimisation of fucoxanthin extraction from Irish seaweeds by response surface methodology. J. Appl. Phycol. 2017, 29, 1027–1036. [Google Scholar] [CrossRef] [Green Version]
  32. Nunes, N.; Leça, J.M.; Pereira, A.C.; Pereira, V.; Ferraz, S.; Barreto, M.C.; Marques, J.C.; de Carvalho, M.A.A.P. Evaluation of fucoxanthin contents in seaweed biomass by vortex-assisted solid-liquid microextraction using high-performance liquid chromatography with photodiode array detection. Algal Res. 2019, 42, 101603. [Google Scholar] [CrossRef]
  33. Yue, Y.; Qiu, Z.D.; Qu, X.Y.; Deng, A.P.; Yuan, Y.; Huang, L.Q.; Lai, C.J.S. Discoursing on Soxhlet extraction of ginseng using association analysis and scanning electron microscopy. J. Pharm. Anal. 2018, 8, 312–317. [Google Scholar] [CrossRef] [PubMed]
  34. Getachew, A.T.; Saravana, P.S.; Cho, Y.J.; Woo, H.C.; Chun, B.S. Concurrent extraction of oil from roasted coffee (Coffea arabica) and fucoxanthin from brown seaweed (Saccharina japonica) using supercritical carbon dioxide. J. CO2 Util. 2018, 25, 137–146. [Google Scholar] [CrossRef]
  35. Shannon, E.; Abu-Ghannam, N. Enzymatic extraction of fucoxanthin from brown seaweeds. Int. J. Food Sci. Technol. 2018, 53, 2195–2204. [Google Scholar] [CrossRef] [Green Version]
  36. Billakanti, J.M.; Catchpole, O.J.; Fenton, T.A.; Mitchell, K.A.; Mackenzie, A.D. Enzyme-assisted extraction of fucoxanthin and lipids containing polyunsaturated fatty acids from Undaria pinnatifida using dimethyl ether and ethanol. Process Biochem. 2013, 48, 1999–2008. [Google Scholar] [CrossRef]
  37. Xiao, X.; Si, X.; Yuan, Z.; Xu, X.; Li, G. Isolation of fucoxanthin from edible brown algae by microwave-assisted extraction coupled with high-speed countercurrent chromatography. J. Sep. Sci. 2012, 35, 2313–2317. [Google Scholar] [CrossRef]
  38. Shang, Y.F.; Kim, S.M.; Lee, W.J.; Um, B.H. Pressurized liquid method for fucoxanthin extraction from Eisenia bicyclis (Kjellman) Setchell. J. Biosci. Bioeng. 2011, 111, 237–241. [Google Scholar] [CrossRef]
  39. Sosa-Hernández, J.E.; Escobedo-Avellaneda, Z.; Iqbal, H.M.N.; Welti-Chanes, J. State-of-the-art extraction methodologies for bioactive compounds from algal biome to meet bio-economy challenges and opportunities. Molecules 2018, 23, 2953. [Google Scholar] [CrossRef] [Green Version]
  40. Roh, M.K.; Uddin, M.S.; Chun, B.S. Extraction of fucoxanthin and polyphenol from Undaria pinnatifida using supercritical carbon dioxide with co-solvent. Biotechnol. Bioprocess Eng. 2008, 13, 724–729. [Google Scholar] [CrossRef]
  41. Sivagnanam, S.P.; Yin, S.; Choi, J.H.; Park, Y.B.; Woo, H.C.; Chun, B.S. Biological properties of fucoxanthin in oil recovered from two brown seaweeds using supercritical CO2 extraction. Mar. Drugs 2015, 13, 3422–3442. [Google Scholar] [CrossRef]
  42. Li, J.; Liu, Y.; Liu, Y.; Wang, Q.; Gao, X.; Gong, Q. Effects of temperature and salinity on the growth and biochemical composition of the brown alga Sargassum fusiforme (Fucales, Phaeophyceae). J. Appl. Phycol. 2019, 31, 3061–3068. [Google Scholar] [CrossRef]
  43. Kanazawa, K.; Ozaki, Y.; Hashimoto, T.; Das, S.K.; Matsushita, S.; Hirano, M.; Okada, T.; Komoto, A.; Mori, N.; Nakatsuka, M. Commercial-scale Preparation of Biofunctional Fucoxanthin from Waste Parts of Brown Sea Algae Laminaria japonica. Food Sci. Technol. Res. 2008, 14, 573–582. [Google Scholar] [CrossRef] [Green Version]
  44. Verma, P.; Kumar, M.; Mishra, G.; Sahoo, D. Multivariate analysis of fatty acid and biochemical constitutes of seaweeds to characterize their potential as bioresource for biofuel and fine chemicals. Bioresour. Technol. 2017, 226, 132–144. [Google Scholar] [CrossRef] [PubMed]
  45. Fraga-Corral, M.; García-Oliveira, P.; Pereira, A.G.; Lourenço-Lopes, C.; Jimenez-Lopez, C.; Prieto, M.A.; Simal-Gandara, J. Technological application of tannin-based extracts. Molecules 2020, 25, 614. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Terasaki, M.; Hirose, A.; Narayan, B.; Baba, Y.; Kawagoe, C.; Yasui, H.; Saga, N.; Hosokawa, M.; Miyashita, K. Evaluation of recoverable functional lipid components of several brown seaweeds (Phaeophyta) from Japan with special reference to fucoxanthin and fucosterol contents. J. Phycol. 2009, 45, 974–980. [Google Scholar] [CrossRef] [PubMed]
  47. Mise, T.; Ueda, M.; Yasumoto, T. Production of fucoxanthin-rich powder from Cladosiphon okamuranus. Adv. J. Food Sci. Technol. 2011, 3, 73–76. [Google Scholar]
  48. Susanto, E.; Fahmi, A.S.; Abe, M.; Hosokawa, M.; Miyashita, K. Lipids, Fatty Acids, and Fucoxanthin Content from Temperate and Tropical Brown Seaweeds. Aquat. Procedia 2016, 7, 66–75. [Google Scholar] [CrossRef]
  49. Agatonovic-Kustrin, S.; Morton, D.W. High-performance thin-layer chromatography HPTLC-direct bioautography as a method of choice for alpha-amylase and antioxidant activity evaluation in marine algae. J. Chromatogr. A 2017, 1530, 197–203. [Google Scholar] [CrossRef]
  50. Heo, S.J.; Yoon, W.J.; Kim, K.N.; Ahn, G.N.; Kang, S.M.; Kang, D.H.; Affan, A.; Oh, C.; Jung, W.K.; Jeon, Y.J. Evaluation of anti-inflammatory effect of fucoxanthin isolated from brown algae in lipopolysaccharide-stimulated RAW 264.7 macrophages. Food Chem. Toxicol. 2010, 48, 2045–2051. [Google Scholar] [CrossRef]
  51. Seely, G.R.; Duncan, M.J.; Vidaver, W.E. Preparative and analytical extraction of pigments from brown algae with dimethyl sulfoxide. Mar. Biol. 1972, 12, 184–188. [Google Scholar] [CrossRef]
  52. Rajauria, G.; Foley, B.; Abu-Ghannam, N. Characterization of dietary fucoxanthin from Himanthalia elongata brown seaweed. Food Res. Int. 2017, 99, 995–1001. [Google Scholar] [CrossRef] [PubMed]
  53. Kang, M.C.; Lee, S.H.; Lee, W.W.; Kang, N.; Kim, E.A.; Kim, S.Y.; Lee, D.H.; Kim, D.; Jeon, Y.J. Protective effect of fucoxanthin isolated from Ishige okamurae against high-glucose induced oxidative stress in human umbilical vein endothelial cells and zebrafish model. J. Funct. Foods 2014, 11, 304–312. [Google Scholar] [CrossRef]
  54. Foo, S.C.; Yusoff, F.M.; Ismail, M.; Basri, M.; Yau, S.K.; Khong, N.M.H.; Chan, K.W.; Ebrahimi, M. Antioxidant capacities of fucoxanthin-producing algae as influenced by their carotenoid and phenolic contents. J. Biotechnol. 2017, 241, 175–183. [Google Scholar] [CrossRef] [PubMed]
  55. Jaswir, I.; Noviendri, D.; Salleh, H.M.; Miyashita, K. Fucoxanthin extractions of brown seaweeds and analysis of their lipid fraction in methanol. Food Sci. Technol. Res. 2012, 18, 251–257. [Google Scholar] [CrossRef] [Green Version]
  56. Jaswir, I.; Noviendri, D.; Salleh, H.M.; Taher, M.; Miyashita, K.; Ramli, N. Analysis of fucoxanthin content and purification of all-trans-fucoxanthin from Turbinaria turbinata and Sargassum plagyophyllum by SiO2 open column chromatography and reversed phase-HPLC. J. Liq. Chromatogr. Relat. Technol. 2013, 36, 1340–1354. [Google Scholar] [CrossRef]
  57. Chen, C.R.; Lin, D.M.; Chang, C.M.J.; Chou, H.N.; Wu, J.J. Supercritical carbon dioxide anti-solvent crystallization of fucoxanthin chromatographically purified from Hincksia mitchellae P.C. Silva. J. Supercrit. Fluids 2017, 119, 1–8. [Google Scholar] [CrossRef]
  58. Raji, V.; Loganathan, C.; Sadhasivam, G.; Kandasamy, S.; Poomani, K.; Thayumanavan, P. Purification of fucoxanthin from Sargassum wightii Greville and understanding the inhibition of angiotensin 1-converting enzyme: An in vitro and in silico studies. Int. J. Biol. Macromol. 2020, 148, 696–703. [Google Scholar] [CrossRef]
  59. Conde, E.; Moure, A.; Domínguez, H. Supercritical CO2 extraction of fatty acids, phenolics and fucoxanthin from freeze-dried Sargassum muticum. J. Appl. Phycol. 2015, 27, 957–964. [Google Scholar] [CrossRef]
  60. Zhu, J.; Sun, X.; Chen, X.; Wang, S.; Wang, D. Chemical cleavage of fucoxanthin from Undaria pinnatifida and formation of apo-fucoxanthinones and apo-fucoxanthinals identified using LC-DAD-APCI-MS/MS. Food Chem. 2016, 211, 365–373. [Google Scholar] [CrossRef]
  61. Kim, S.M.; Shang, Y.F.; Um, B.H. A preparative method for isolation of fucoxanthin from Eisenia bicyclis by centrifugal partition chromatography. Phytochem. Anal. 2011, 22, 322–329. [Google Scholar] [CrossRef]
  62. Sangeetha, R.K.; Bhaskar, N.; Divakar, S.; Baskaran, V. Bioavailability and metabolism of fucoxanthin in rats: Structural characterization of metabolites by LC-MS (APCI). Mol. Cell. Biochem. 2010. [Google Scholar] [CrossRef] [PubMed]
  63. Sun, P.; Wong, C.C.; Li, Y.; He, Y.; Mao, X.; Wu, T.; Ren, Y.; Chen, F. A novel strategy for isolation and purification of fucoxanthinol and fucoxanthin from the diatom Nitzschia laevis. Food Chem. 2019, 277, 566–572. [Google Scholar] [CrossRef] [PubMed]
  64. Rajauria, G.; Abu-Ghannam, N. Isolation and partial characterization of bioactive fucoxanthin from Himanthalia elongata brown seaweed: A TLC-based approach. Int. J. Anal. Chem. 2013, 2013, 87–107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Yip, W.H.; Lim, S.J.; Mustapha, W.A.W.; Maskat, M.Y.; Said, M. Characterisation and stability of pigments extracted from Sargassum binderi obtained from Semporna, Sabah. Sains Malays. 2014, 43, 1345–1354. [Google Scholar]
  66. Pardilhó, S.L.; Machado, S.F.; Bessada, S.M.F.; Almeida, M.; Oliveira, M.B.; Dias, J.M. Marine Macroalgae Waste from Northern Portugal: A Potential Source of Natural Pigments? Waste Biomass Valoriz. 2020, 1–10. [Google Scholar] [CrossRef]
  67. Mohibbullah, M.; Haque, M.N.; Khan, M.N.A.; Park, I.-S.; Moon, I.S.; Hong, Y.-K. Neuroprotective effects of fucoxanthin and its derivative fucoxanthinol from the phaeophyte Undaria pinnatifida attenuate oxidative stress in hippocampal neurons. J. Appl. Phycol. 2018, 30, 3243–3252. [Google Scholar] [CrossRef]
  68. Strand, A.; Herstad, O.; Liaaen-Jensen, S. Fucoxanthin metabolites in egg yolks of laying hens. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 1998. [Google Scholar] [CrossRef]
  69. Goiris, K.; Muylaert, K.; Fraeye, I.; Foubert, I.; De Brabanter, J.; De Cooman, L. Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. J. Appl. Phycol. 2012, 24, 1477–1486. [Google Scholar] [CrossRef]
  70. Lichtenthaler, H.K.; Buschmann, C. Chlorophylls and Carotenoids: Measurement and Characterization by UV-VIS Spectroscopy. Curr. Protoc. Food Anal. Chem. 2001, 1, F4.3.1–F4.3.8. [Google Scholar] [CrossRef]
  71. Li, F.L.; Wang, L.J.; Fan, Y.; Parsons, R.L.; Hu, G.R.; Zhang, P.Y. A rapid method for the determination of fucoxanthin in diatom. Mar. Drugs 2018, 16, 33. [Google Scholar] [CrossRef] [Green Version]
  72. Sudhakar, M.P.; Ananthalakshmi, J.S.; Nair, B.B. Extraction, purification and study on antioxidant properties of fucoxanthin from brown seaweeds. J. Chem. Pharm. Res. 2013, 5, 169–175. [Google Scholar]
  73. Gómez-Loredo, A.; González-Valdez, J.; Rito-Palomares, M. Insights on the downstream purification of fucoxanthin, a microalgal carotenoid, from an aqueous two-phase system stream exploiting ultrafiltration. J. Appl. Phycol. 2015, 27, 1517–1523. [Google Scholar] [CrossRef]
  74. Li, H.; Xu, Y.; Sun, X.; Wang, S.; Wang, J.; Zhu, J.; Wang, D.; Zhao, L. Stability, bioactivity, and bioaccessibility of fucoxanthin in zein-caseinate composite nanoparticles fabricated at neutral pH by antisolvent precipitation. Food Hydrocoll. 2018, 84, 379–388. [Google Scholar] [CrossRef]
  75. Koo, S.Y.; Mok, I.-K.; Pan, C.-H.; Kim, S.M. Preparation of Fucoxanthin-Loaded Nanoparticles Composed of Casein and Chitosan with Improved Fucoxanthin Bioavailability. J. Agric. Food Chem. 2016, 64, 9428–9435. [Google Scholar] [CrossRef] [PubMed]
  76. Sun, X.; Xu, Y.; Zhao, L.; Yan, H.; Wang, S.; Wang, D. The stability and bioaccessibility of fucoxanthin in spray-dried microcapsules based on various biopolymers. RSC Adv. 2018, 8, 35139–35149. [Google Scholar] [CrossRef] [Green Version]
  77. Ye, L.; Eitenmiller, R.R. Fat-soluble vitamins. In Handbook of Food Science, Technology, and Engineering—4 Volume Set; CRC: Boca Raton, FL, USA, 2005; ISBN 9781466507876. [Google Scholar]
  78. López, C.J.; Caleja, C.; Prieto, M.A.; Sokovic, M.; Calhelha, R.C.; Barros, L.; Ferreira, I.C.F.R. Stability of a cyanidin-3-O-glucoside extract obtained from Arbutus unedo L. and incorporation into wafers for colouring purposes. Food Chem. 2019, 275, 426–438. [Google Scholar] [CrossRef] [Green Version]
  79. Prieto, M.A.; Murado, M.A.; Rodríguez-Amado, I.; Vázquez, J.A. β-Carotene assay revisited. Application to characterize and quantify antioxidant and prooxidant activities in a microplate. J. Agr. Food Chem. 2012, 60, 8983–8993. [Google Scholar] [CrossRef] [Green Version]
  80. Mok, I.K.; Lee, J.K.; Kim, J.H.; Pan, C.H.; Kim, S.M. Fucoxanthin bioavailability from fucoxanthin-fortified milk: In vivo and in vitro study. Food Chem. 2018, 258, 79–86. [Google Scholar] [CrossRef]
  81. Wang, X.; Li, H.; Wang, F.; Xia, G.; Liu, H.; Cheng, X.; Kong, M.; Liu, Y.; Feng, C.; Chen, X.; et al. Isolation of fucoxanthin from Sargassum thunbergii and preparation of microcapsules based on palm stearin solid lipid core. Front. Mater. Sci. 2017, 11, 66–74. [Google Scholar] [CrossRef]
  82. Ma, Z.; Khalid, N.; Shu, G.; Zhao, Y.; Kobayashi, I.; Neves, M.A.; Tuwo, A.; Nakajima, M. Fucoxanthin-Loaded Oil-in-Water Emulsion-Based Delivery Systems: Effects of Natural Emulsifiers on the Formulation, Stability, and Bioaccessibility. ACS Omega 2019, 4, 10502–10509. [Google Scholar] [CrossRef]
  83. Salvia-Trujillo, L.; Sun, Q.; Um, B.H.; Park, Y.; McClements, D.J. In Vitro and in vivo study of fucoxanthin bioavailability from nanoemulsion-based delivery systems: Impact of lipid carrier type. J. Funct. Foods 2015. [Google Scholar] [CrossRef] [Green Version]
  84. Zhao, D.; Yu, D.; Kim, M.; Gu, M.Y.; Kim, S.M.; Pan, C.H.; Kim, G.H.; Chung, D. Effects of temperature, light, and pH on the stability of fucoxanthin in an oil-in-water emulsion. Food Chem. 2019, 291, 87–93. [Google Scholar] [CrossRef] [PubMed]
  85. Ravi, H.; Baskaran, V. Biodegradable chitosan-glycolipid hybrid nanogels: A novel approach to encapsulate fucoxanthin for improved stability and bioavailability. Food Hydrocoll. 2015, 43, 717–725. [Google Scholar] [CrossRef]
  86. Taofiq, O.; Heleno, S.A.; Calhelha, R.C.; Fernandes, I.P.; Alves, M.J.; Barros, L.; González-Paramás, A.M.; Ferreira, I.C.F.R.; Barreiro, M.F. Mushroom-based cosmeceutical ingredients: Microencapsulation and in vitro release profile. Ind. Crops Prod. 2018, 124, 44–52. [Google Scholar] [CrossRef] [Green Version]
  87. Wang, L.; Park, Y.J.; Jeon, Y.J.; Ryu, B.M. Bioactivities of the edible brown seaweed, Undaria pinnatifida: A review. Aquaculture 2018, 495, 873–880. [Google Scholar] [CrossRef]
  88. Miyashita, K.; Hosokawa, M. Fucoxanthin in the management of obesity and its related disorders. J. Funct. Foods 2017, 36, 195–202. [Google Scholar] [CrossRef]
  89. Maeda, H.; Tsukui, T.; Sashima, T.; Hosokawa, M.; Miyashita, K. Seaweed carotenoid, fucoxanthin, as a multi-functional nutrient. Asia Pac. J. Clin. Nutr. 2008, 17, 196–199. [Google Scholar]
  90. Gumus, R.; Urcar Gelen, S.; Koseoglu, S.; Ozkanlar, S.; Ceylan, Z.G.; Imik, H. The effects of fucoxanthin dietary inclusion on the growth performance, antioxidant metabolism and meat quality of broilers. Rev. Bras. Cienc. Avic. 2018, 20, 487–496. [Google Scholar] [CrossRef]
  91. Zhang, L.; Wang, H.; Fan, Y.; Gao, Y.; Li, X.; Hu, Z.; Ding, K.; Wang, Y.; Wang, X. Fucoxanthin provides neuroprotection in models of traumatic brain injury via the Nrf2-ARE and Nrf2-autophagy pathways. Sci. Rep. 2017, 7, 1–15. [Google Scholar] [CrossRef] [Green Version]
  92. Hu, L.; Chen, W.; Tian, F.; Yuan, C.; Wang, H.; Yue, H. Neuroprotective role of fucoxanthin against cerebral ischemic/reperfusion injury through activation of Nrf2/HO-1 signaling. Biomed. Pharmacother. 2018, 106, 1484–1489. [Google Scholar] [CrossRef]
  93. Zhao, D.; Kim, S.M.; Pan, C.H.; Chung, D. Effects of heating, aerial exposure and illumination on stability of fucoxanthin in canola oil. Food Chem. 2014, 145, 505–513. [Google Scholar] [CrossRef] [PubMed]
  94. Robertson, R.C.; Gracia Mateo, M.R.; O’Grady, M.N.; Guihéneuf, F.; Stengel, D.B.; Ross, R.P.; Fitzgerald, G.F.; Kerry, J.P.; Stanton, C. An assessment of the techno-functional and sensory properties of yoghurt fortified with a lipid extract from the microalga Pavlova lutheri. Innov. Food Sci. Emerg. Technol. 2016, 37, 237–246. [Google Scholar] [CrossRef]
  95. Mok, I.K.; Yoon, J.R.; Pan, C.H.; Kim, S.M. Development, quantification, method validation, and stability study of a novel fucoxanthin-fortified milk. J. Agric. Food Chem. 2016, 64, 6196–6202. [Google Scholar] [CrossRef] [PubMed]
  96. Sugimura, R.; Suda, M.; Sho, A.; Takahashi, T.; Sashima, T.; Abe, M.; Hosokawa, M.; Miyashita, K. Stability of fucoxanthin in dried Undaria pinnatifida (wakame) and baked products (scones) containing wakame powder. Food Sci. Technol. Res. 2012, 18, 687–693. [Google Scholar] [CrossRef] [Green Version]
  97. Sasaki, K.; Ishihara, K.; Oyamada, C.; Sato, A.; Fukushi, A.; Arakane, T.; Motoyama, M.; Yamazaki, M.; Mitsumoto, M. Effects of fucoxanthin addition to ground chicken breast meat on lipid and colour stability during chilled storage, before and after cooking. Asian-Australas. J. Anim. Sci. 2008, 21, 1067–1072. [Google Scholar] [CrossRef]
  98. Matsui, M.; Tanaka, K.; Higashiguchi, N.; Okawa, H.; Yamada, Y.; Tanaka, K.; Taira, S.; Aoyama, T.; Takanishi, M.; Natsume, C.; et al. Protective and therapeutic effects of fucoxanthin against sunburn caused by UV irradiation. J. Pharmacol. Sci. 2016, 132, 55–64. [Google Scholar] [CrossRef] [Green Version]
  99. Heo, S.J.; Jeon, Y.J. Protective effect of fucoxanthin isolated from Sargassum siliquastrum on UV-B induced cell damage. J. Photochem. Photobiol. B Biol. 2009, 95, 101–107. [Google Scholar] [CrossRef]
  100. Shimoda, H.; Tanaka, J.; Shan, S.J.; Maoka, T. Anti-pigmentary activity of fucoxanthin and its influence on skin mRNA expression of melanogenic molecules. J. Pharm. Pharmacol. 2010. [Google Scholar] [CrossRef]
  101. Rodríguez-Luna, A.; Ávila-Román, J.; González-Rodríguez, M.L.; Cózar, M.J.; Rabasco, A.M.; Motilva, V.; Talero, E. Fucoxanthin-containing cream prevents epidermal hyperplasia and UVB-induced skin erythema in mice. Mar. Drugs 2018, 16, 378. [Google Scholar] [CrossRef] [Green Version]
  102. Lee, Y.-J.; Nam, G.-W. Sunscreen boosting effect by solid lipid nanoparticles-loaded fucoxanthin formulation. Cosmetics 2020, 7, 14. [Google Scholar] [CrossRef] [Green Version]
Foods 09 01113 g001 550
Figure 1. General overview of the sources of fucoxanthin, extraction and quantification/identification techniques, purification systems and stabilization studies for further industrial application of this compound. The definition for the abbreviations used in this figure can be seen in the abbreviation list provided. Extraction methods and conditions: Maceration extraction (ME); Vortex-assisted solid-liquid micro-extraction (VAE); Enzyme assisted extraction (EAE); Microwave-assisted extraction (MAE); Ultrasound-assisted extraction (UAE); Pressurized liquid extraction (PLE); Supercritical fluid extraction (SFE). Detection method: High Performance Liquid Chromatography (HPLC); HPLC with diode array detector (HPLC-DAD); HPLC with ultraviolet detector (HPLC-UV); Liquid Chromatography-Mass Spectrometry (LC-MS); Nuclear Magnetic Resonance (1H-NMR); Fourier Transform-Infrared Spectroscopy (FTIR).
Figure 1. General overview of the sources of fucoxanthin, extraction and quantification/identification techniques, purification systems and stabilization studies for further industrial application of this compound. The definition for the abbreviations used in this figure can be seen in the abbreviation list provided. Extraction methods and conditions: Maceration extraction (ME); Vortex-assisted solid-liquid micro-extraction (VAE); Enzyme assisted extraction (EAE); Microwave-assisted extraction (MAE); Ultrasound-assisted extraction (UAE); Pressurized liquid extraction (PLE); Supercritical fluid extraction (SFE). Detection method: High Performance Liquid Chromatography (HPLC); HPLC with diode array detector (HPLC-DAD); HPLC with ultraviolet detector (HPLC-UV); Liquid Chromatography-Mass Spectrometry (LC-MS); Nuclear Magnetic Resonance (1H-NMR); Fourier Transform-Infrared Spectroscopy (FTIR).
Foods 09 01113 g001
Foods 09 01113 g002 550
Figure 2. Human health benefits of fucoxanthin.
Figure 2. Human health benefits of fucoxanthin.
Foods 09 01113 g002
Table
Table 1. Brown algae species described as a source of fucoxanthin extracted by conventional extraction techniques, detection methods employed for determining its presence and quantification values (fucoxanthin concentration are expressed in fucoxanthin (Fx) mg/g of DW, or where not determined, “nd” was indicated).
Table 1. Brown algae species described as a source of fucoxanthin extracted by conventional extraction techniques, detection methods employed for determining its presence and quantification values (fucoxanthin concentration are expressed in fucoxanthin (Fx) mg/g of DW, or where not determined, “nd” was indicated).
Algae SpeciesSolventExtraction ConditionsDetection MethodFx (mg/g DW)Ref.
ME
Alaria crassifoliaMeOHRT, 12 hHPLC-PDA1.10[46]
Alaria esculentaAcO 62.2%30 °C, 36.5 minHPLC-DAD0.87[31]
Analipus japonicasMeOHRT, 12 hHPLC-PDA1.40[46]
Cladosiphon okamuranusMeOHRT, 1 hHPLC-DAD0.27[47]
Cystoseira hakodatensisCh, MeOH (1:2)RT, 2 hHPLC-DAD2.01[48]
MeOHRT, 12 hHPLC-PDA2.40[46]
Ch/MeOH (1:2)RT, 1 hHPLC-DAD3.47[24]
Desmarestia viridisMeOHRT, 12 hHPLC-PDA0.10[46]
Dictyopteris australisAcO4 °C, 12 hSpec0.23[44]
Dictyota dichotomaEtOHRT, 15 min × 5HPTLC0.44[49]
AcO4 °C, 12 hSpec0.18[44]
MeOHRT, 24 hHPLC-PDA6.42[50]
Ecklonia kuromeChl/MeOH (1:2)RT, 2 hHPLC-DAD1.68[48]
Fucus distichusMeOHRT, 12 hHPLC-PDA0.90[46]
AcORT, 5 minSpec0.16[51]
Fucus serratusHx/AcO (70:30)RT, 24 hHPLC-DAD3.57[27]
Himanthalia elongatan-Hx, DE, ChRT, 15 minLC-ESI-MS, HPLC, 1H-NMR18.60[52]
Hizikia fusiformisMeOH-HPLC-DAD0.02[43]
Ishige okamuraeMeOH HPLC-DADnd[53]
Iyengaria stellateAcO4 °C, 12 hSpec0.18[44]
Kjellmaniella crassifoliaMeOHRT, 15 minHPLC-DAD0.15[54]
Laminaria japonicaMeOH-HPLC-DAD0.19[43]
Laminaria digitataAcO 62.2%30°, 36.5 minHPLC-DAD0.65[31]
Laminaria religiosaMeOHRT, 96 hHPLC-DAD, 1H-NMR, 13C-NMR0.24[21]
Laminaria saccharinaAcORT, 5 minSpec0.24[51]
Leathesia difformisMeOHRT, 12 hHPLC-PDA0.30[46]
Lobophora variegataAcO4 °C, 12 hSpec0.23[44]
Melanosiphon intestinalisMeOHRT, 12 hHPLC-PDA1.90[46]
Myagropsis myagroidesMeOHRT, 24 hHPLC-PDA9.01[50]
Padina australisChl/MeOH (1:2)RT, 2 hHPLC-DAD1.29[48]
Padina gymnosporaAcO4 °C, 12 hSpec0.43[44]
Padina minorEtOHRT, 15 min × 5HPTLC0.50[49]
Padina pavonica0.43
Padina tetrastromaticaAcO4 °C, 12 hSpec0.41[44]
Petalonia binghamiaeMeOHRT, 48 hHPLC-DAD, 1H-NMR, 13C-NMR0.58[21]
Saccharina japonicaMeOHRT, 15 minHPLC-DAD0.03[54]
Saccharina sculperaMeOHRT, 12 hHPLC-PDA0.70[46]
Sargassum binderiMeOHRT, 12 h × 2HPLC-DAD0.73[55]
Sargassum confusumMeOHRT, 12 hHPLC-PDA1.60[46]
Sargassum crassifoliumChl/MeOH (1:2)RT, 2 hHPLC-DAD1.64[48]
Sargassum duplicatumMeOHRT, 12 h × 2HPLC-DAD1.01[55]
Sargassum fulvellumMeOH-HPLC-DAD0.01 *[43]
Sargassum fusiformeMeOHRT, 12 hHPLC-PDA1.10[46]
AcO/EtOH (1:40)65 °C, 80 minSpec2.62[42]
Sargassum horneriChl/MeOH (1:2)RT, 2 hHPLC-DAD2.12[48]
MeOHRT, 12 hHPLC-PDA3.70[46]
Ch/MeOH (1:2)RT, 1 hHPLC-DAD4.49 [24]
Sargassum linearifoliumAcO4 °C, 12 hSpec0.37[44]
Sargassum muticumAcORT, 5 minSpec0.29[51]
Sargassum plagiophyllumAcO/MeOH (7:3)ice, 15 minHPLC0.71 [56]
Sargassum polycystumEtOHRT, 15 min × 5HPTLC0.41[49]
Sargassum siliquastrumChl/MeOH (1:2)RT, 2 hHPLC-DAD1.99[48]
Sargassum thunbergiiMeOHRT, 12 hHPLC-PDA1.80[46]
Scytosiphon lomentariaMeOHRT, 12 hHPLC-PDA0.50[46]
MeOHRT, 96 hHPLC-DAD, 1H-NMR, 13C-NMR0.56[21]
Silvetia babingtoniiMeOHRT, 12 hHPLC-PDA0.70[46]
Spatoglossum asperumAcO4 °C, 12 hSpec0.58[44]
Sphaerotrichia divaricataMeOHRT, 12 hHPLC-PDA0.20[46]
Stoechospermum marginatumAcO4 °C, 12 hSpec0.37[44]
Turbinaria ornateChl/MeOH (1:2)RT, 2 hHPLC-DAD1.27[48]
Turbinaria spp.AcO4 °C, 12 hSpec0.43[44]
Turbinaria turbinataAcO/MeOH (7:3)ice, 15 minHPLC0.59[56]
Undaria pinnatifidaMeOHRT, 96 hHPLC-DAD, 1H-NMR, 13C-NMR2.67[21]
MeOHRT, 1 hHPLC-DAD2.08[22]
MeOHRT, 1 hHPLC-DAD4.96 *
EtOHRT, 1 hHPLC-DAD0.70[36]
VAE
Ascophylum nodossumEtOHRT, 15 minHPLC-PDA0.02[32]
Dictyota dichotoma0.60
Fucus vesiculosusEtOHRT, 15 minHPLC-PDA0.02[32]
AcO40 °C, 40 minHPLC-DAD0.70[31]
Sargassum vulgareEtOHRT, 15 minHPLC-PDA0.40[32]
Zonaria tournefortii0.80
SAE
Feldmannia mitchelliaeEA80 °C, 16 hHPLC5.50[57]
Saccharina japonican-Hx40 °C, 16 hHPLC0.45[34]
Sargassum swartzii C. AgardhEA80 °C, 6 hFT-IR, 1H-NMR, 13C-NMR0.17[58]
EAE
Fucus vesiculosusWViscozyme, 50 °C, 100 rpm, 10 minHPLC-UV, LC-MS0.66[35]
MAE
Laminaria japonicaHp, AcO, W50 °C, 10 minLC-ESI-MS, HPLC, 1H-NMR0.04[37]
Sargassum fusiforme0.02
Undaria pinnatifida0.90
UEA
Padina tetrastromaticaEtOH50 Hz, 30 minHPLC-DAD0.75[20]
PLE
Eisenia bicyclisEtOH110 °C, 5 minHPLC-PDA0.42[38]
Undaria pinnatifidaEtOH78 °C, 12 hHPLC-UV0.05[19]
SFE
Fucus serratusEtOH50 °C, 304 bars, 1 hHPLC-DAD2.18[27]
Sargassum horneriCO2, EtOH45 °C, 250 barsHPLC-DAD0.77[41]
Sargassum japonica0.41
Sargassum muticumCO2, EtOH50 °C, 100 barsHPLC-DAD0,55[59]
Undaria pinnatifidaCO2, EtOH50 °C, 200 barsHPLC-UV<0.01[40]
CO2, EtOH60 °C, 400 barsHPLC-UV0.99[19]
Solvent: Ethanol (EtOH); Methanol (MeOH); Acetone (AcO); Chloroform (Ch); Hexane (Hx); n-Hexane (n-Hx); Diethyl ether (DE), Ethyl Acetate (EA); Water (W); Heptane (Hp); Carbon dioxide (CO2). Extraction methods and conditions: Maceration extraction (ME); Vortex-assisted solid-liquid micro-extraction (VAE); Room temperature (RT); Soxhlet-assisted Extraction (SAE); Enzyme assisted extraction (EAE); Microwave-assisted extraction (MAE); Ultrasound-assisted extraction (UAE); Pressurized liquid extraction (PLE); Supercritical fluid extraction (SFE). Detection method: High Performance Liquid Chromatography (HPLC); HPLC with diode array detector (HPLC-DAD); HPLC with ultraviolet detector (HPLC-UV); High Performance Thin Layer Chromatography (HPTLC); Liquid Chromatography-Atmospheric Pressure Chemical Ionization coupled to Mass Spectrometry (LC-APCI-MS); Liquid Chromatography-Electrospray Ionization coupled to Mass Spectrometry (LC-ESI-MS); Carbon-13 nuclear magnetic resonance (13C-NMR); Proton nuclear magnetic resonance (1H-NMR); Spectrophotometry (Spec); Fourier Transform-Infrared Spectroscopy (FT-IR). Fucoxanthin content: not determined: fucoxanthin was found but not quantified (nd); Dry Weight (DW); Fresh Weight (* FW).

Share and Cite

MDPI and ACS Style

Lourenço-Lopes, C.; Garcia-Oliveira, P.; Carpena, M.; Fraga-Corral, M.; Jimenez-Lopez, C.; Pereira, A.G.; Prieto, M.A.; Simal-Gandara, J. Scientific Approaches on Extraction, Purification and Stability for the Commercialization of Fucoxanthin Recovered from Brown Algae. Foods 2020, 9, 1113. https://doi.org/10.3390/foods9081113

AMA Style

Lourenço-Lopes C, Garcia-Oliveira P, Carpena M, Fraga-Corral M, Jimenez-Lopez C, Pereira AG, Prieto MA, Simal-Gandara J. Scientific Approaches on Extraction, Purification and Stability for the Commercialization of Fucoxanthin Recovered from Brown Algae. Foods. 2020; 9(8):1113. https://doi.org/10.3390/foods9081113

Chicago/Turabian Style

Lourenço-Lopes, Catarina, Paula Garcia-Oliveira, Maria Carpena, Maria Fraga-Corral, Cecilia Jimenez-Lopez, Antia G. Pereira, Miguel A. Prieto, and Jesus Simal-Gandara. 2020. "Scientific Approaches on Extraction, Purification and Stability for the Commercialization of Fucoxanthin Recovered from Brown Algae" Foods 9, no. 8: 1113. https://doi.org/10.3390/foods9081113

APA Style

Lourenço-Lopes, C., Garcia-Oliveira, P., Carpena, M., Fraga-Corral, M., Jimenez-Lopez, C., Pereira, A. G., Prieto, M. A., & Simal-Gandara, J. (2020). Scientific Approaches on Extraction, Purification and Stability for the Commercialization of Fucoxanthin Recovered from Brown Algae. Foods, 9(8), 1113. https://doi.org/10.3390/foods9081113

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop