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Hossain, A. Northern Sea Cucumber. Encyclopedia. Available online: https://encyclopedia.pub/entry/18280 (accessed on 26 June 2024).
Hossain A. Northern Sea Cucumber. Encyclopedia. Available at: https://encyclopedia.pub/entry/18280. Accessed June 26, 2024.
Hossain, Abul. "Northern Sea Cucumber" Encyclopedia, https://encyclopedia.pub/entry/18280 (accessed June 26, 2024).
Hossain, A. (2022, January 14). Northern Sea Cucumber. In Encyclopedia. https://encyclopedia.pub/entry/18280
Hossain, Abul. "Northern Sea Cucumber." Encyclopedia. Web. 14 January, 2022.
Northern Sea Cucumber
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This entry is adapted from the peer-reviewed paper 10.3390/md18050274

Sea cucumber (Cucumaria frondosa) is the most abundant and widely distributed species in the cold waters of North Atlantic Ocean. C. frondosa contains a wide range of bioactive compounds, mainly collagen, cerebrosides, glycosaminoglycan, chondroitin sulfate, saponins, phenols, and mucopolysaccharides, which demonstrate unique biological and pharmacological properties. In particular, the body wall of this marine invertebrate is the major edible part and contains most of the active constituents, mainly polysaccharides and collagen, which exhibit numerous biological activities, including anticancer, anti-hypertensive, anti-angiogenic, anti-inflammatory, antidiabetic, anti-coagulation, antimicrobial, antioxidation, and anti- osteoclastogenic properties.

Cucumaria frondosa geographical distribution market bioactive compounds Atlantic sea cucumber

1. Introduction

Sea cucumber belongs to the class of Holothuroidea and the phylum of Echinodermata; it is globally found in deep seas and benthic areas. Due to multiple biological activities, it has been widely consumed in China, Korea, Japan, Malaysia, Indonesia, and Russia. It has a leathery skin and a soft and cylindrical body containing a single branched gonad. Sea cucumber contains very low fat and cholesterol, but a high protein content [1]. There are around 1500 species of sea cucumber found around the world [2] and about 100 of them are well known for human consumption [3]. The most important commercial species are Apostichopus japonicus, Acaudina molpadioides, Actinopyga mauritiana, Cucumaria frondosa, Cucumaria japonica, Holothuria forskali, Holothuria polii, Holothuria nobilis, Holothuria tubulosa, Isostichopus badionotus, and Pearsonothuria graeffei. The most common sea cucumbers found in the North Pacific and North Atlantic areas are Cucumaria frondosa, Parastichopus californicus, Cucumaria japonica, and Parastichopus parvimensis. In particular, Cucumaria frondosa is known as orange-footed sea cucumber, which is the most abundant and broadly distributed species along the east coast of Canada.
Sea cucumber has received greater attention due to its potential therapeutic benefits and as a marine food product. In addition, it has gained increasing interest as a functional food ingredient due to the availability of its biologically active compounds with medicinal properties. Sea cucumber has an impressive nutritional profile including protein (mainly collagen), lipid (mostly omega-3 and omega-6 fatty acids), vitamins A, B1 (thiamine), B2 (riboflavin), B3 (niacin), and minerals, mainly magnesium, zinc, calcium, and iron [4][5][6][7][8]. Moreover, it contains numerous bioactive compounds, namely saponins [9], glycosaminoglycans [10], chondroitin sulfate [11], sulfated polysaccharides [12][13], fucoidan [14][15], phenolics [16], peptides [17], lectins [18], cerebrosides [19][20], sterols [21], and both the omega-3 and omega-6 fatty acids [22]. As a result, it has been used as a tonic food and folk medicine in Eastern Asia to cure numerous ailments.
East Asian consumers consider sea cucumber as the most luxurious and nutritious food and have used it as a traditional remedy to cure hypertension, rheumatism, asthma, cuts and burns, joint pain, back pain, wound injuries, kidney problem, reproductive disorder, impotence, and constipation [1][23]. The chemical compounds isolated from different sea cucumbers demonstrate unique biological and pharmacological properties such as anticancer [4][24][25], anti-angiogenic [26], anticoagulant [10][27][28], anti-inflammatory [29][30], anti-hypertension [31], antimicrobial [32][33], antithrombotic [28], antioxidant [34][35], antitumor [29], as well as wound healing activities [36]. Particularly, glycosaminoglycan from C. frondosa shows heparin-like anticoagulant activity [37]. In addition, sea cucumber-derived bioactive components can be applied to the mouth, face, hands, feet, hair, nails, joints, scalp, and different sensitive body parts as novel cosmetic ingredients [38]. Moreover, dry tablets obtained from the body wall of sea cucumber are broadly used in Asia and the USA for physiological and nutraceutical benefits, particularly for improving sexual performance [5]. In addition, people of Malaysia consume sea cucumber skin extracts to cure hypertension, asthma, wound healing, cuts, and burns [39][40]. Despite the growing interest and demand in sea cucumber, C. frondosa has not yet been fully explored compared to other species for potential use as a nutraceutical and functional food ingredient.

2. Description, Growth, and Distribution

The orange-footed sea cucumber (C. frondosa) is widely distributed in the north Atlantic, mainly in the nearshore parts, and in the Barents Sea along the coast of the Russian Federation. They are soft-bodied, cucumber-like, with leathery skin, elongated, and worm-like body. The mouth is surrounded by aquapharyngeal bulb/tentacles/flower at one end of the body and an anus at the opposite end (Figure 1). It can grow to a maximum length of 40–50 cm, a width of 10–15 cm, and a weight of 100 to 500 g. The body wall is the main part (up to 50% of the total body weight) of this species, which contains around 85% moisture. Generally, sea cucumbers eat mud or dead particle remains; however, C. frondosa feed on phytoplankton, zooplankton, and organic matter by spreading out their tentacles [41][42].
Figure 1. Body parts of Cucumaria frondosa.
Interestingly, this species can regenerate or renew themselves very quickly, and they may have the ability to restore their lost organs [43]. Sea cucumbers contain collagen (echinoderms collagen) in their skin, so they are able to change their mechanical state (liquid/jelly to solid form) very quickly [44] and, hence, use it as a possible defense mechanism. Moreover, it is assumed that they control their movement by thousands of tiny tube feet and communicate with each other by transferring hormone signals through the water. Due to the plasticity of their physical characteristics, morphometrics, including length, weight, and age are quite challenging to determine [45]. Generally, C. frondosa (orange footed sea cucumber), pumpkins or phenix sea cucumber are harvested from May to November in Atlantic Canada. Moreover, the growth rate of C. frondosa is slower compared to other sea cucumber species with an average growth rate of 2 mm per month. Furthermore, the growth rate is dependent on temperature, light, salinity, depth, and level of disturbance [46]. However, due to the small size and thin body wall, C. frondosa is still considered a low-grade product compared to other commercial species of sea cucumber [47].
The distribution of C. frondosa ranges from the eastern coast of Canada (Gulf from the lower tide limit to the deepest area and St. Lawrence Estuary), southwest coast of New England, down to the coast of northern Europe, southern Iceland, and the coast of Greenland, Scandinavia, and the Faroe Islands (Figure 2). Particularly, it is found from lower inter-tidal and cold tide-pools to sub-tidal down to 1000 ft and from the Arctic to Cape Cod. These sea cucumbers are most abundant at strong currents and depths region (30 to 300 m), and they prefer to live in rocky (corals and seaweeds) or in mixed substrates (stone, sand, gravel, and shells) [48][49][50].
Figure 2. Distribution of the Northern sea cucumber (Cucumaria frondosa).

3. Proximate Composition

Very few studies have so far been performed on the proximate composition of C. frondosa. From a nutritional point of view, C. frondosa is an ideal tonic food and has an impressive nutritional profile such as vitamins, minerals, carbohydrates, amino acids, and fatty acids. Zhong, Khan, and Shahidi [51] reported that the content of moisture, protein, lipid, ash, and carbohydrate in fresh whole sea cucumber were approximately 90.5, 5.5, 0.8, 3.5, and 1.5%, respectively. Both essential and non-essential amino acids (17 of them) were present along with a high amount of free amino acids. In particular, fresh whole sea cucumber contains glutamic acid (57.5 mg/g), lysine (30.6 mg/g), leucine (28.3 mg/g), glycine (29.8 mg/g), asparagine (27.8 mg/g), along with a considerable amount of alanine, arginine, proline, and valine. However, fresh whole sea cucumber had lower amino acids and fatty acids contents than those with internal organs removed (Table 1). Moreover, eicosapentaenoic acid (EPA) was the predominant fatty acid in C. frondosa compared to docosahexaenoic acid (DHA). On the other hand, Mamelona, Saint-Louis, and Pelletier [52] stated that Atlantic sea cucumber viscera contained approximately 92.3% moisture, 4.5% protein, 2% fat, 0.7% ash, and 0.3% carbohydrate. Most of the essential and non-essential amino acids were also present with a high amount of glutamic acid, aspartic acid, and arginine. Moreover, Atlantic sea cucumber viscera are a rich source of polyunsaturated fatty acids (PUFA, about 44%) with 24% saturated fatty acids (SFA) and 30% monounsaturated fatty acids (MUFA). The gonad and muscle tissues of C. frondosa had a significantly higher amount of lipid and fatty acids (EPA and DHA) compared to other body parts [50]. They also reported that a considerable amount of lipids (3.40 ± 0.28 mg/g w/w); mainly DHA, palmitic acid, and EPA was present when C. frondosa fed on a fish eggs diet. However, viscera contained a high level of essential (Cu, Fe, Zn, K, Na, Mn, As, Mg, Se, Ni, and Ca) and a very small amount non-essential (Cd, Co, and Pb) trace elements, and vitamins (niacin, pantothenic acid, alpha-tocopherol, riboflavin, thiamine, and folates). Theses minerals stimulate the metabolism of the body, promote healthy growth, and assist in lowering the blood sugar level [52]. Therefore, C. frondosa is considered as a rich source of nutrients, including vitamins, and minerals, in the marine food industry.
Table 1. Total amino acid profile and fatty acid composition of fresh Atlantic sea cucumber.

Amino acids

Sea cucumber with viscera (mg/g) a

Body wall (mg/g) a

Viscera (%) b

Fatty Acids

Sea cucumber with viscera (%) a

Body wall (%) a

Viscera (%) b

Valine

16.8

19.7

5.4

14:00

1.8

1.88

10.1

Methionine

9.4

10.3

2.3

15:00

4.03

2.18

0.3

Isoleucine

12.6

13.9

4.7

16:00

2.83

2.33

13.3

Leucine

28.3

30.8

7.2

16:1 n-7

7.36

5.75

6

Phenylalanine

13.1

17.8

3.5

17:1 n-7

2.44

3.87

N/A

Histidine

3.3

2.8

2.3

18:00

4.2

5.41

2.1

Threonine

10.9

12.9

5

18:1 n-9

3.72

2.43

4.9

Lysine

30.6

29.1

6.6

18:1 n-7

3.37

3.52

N/A

Aspartic acid

27.8

39.1

10

20:1 n-9

1.66

4

N/A

Glutamic acid

57.5

66.4

14.3

20:3 n-3

2.54

5

2.5

Serine

15.5

19.3

4.3

20:5 n-3

43.2

46.1

17.1

Glycine

29.8

56.1

8

22:00

2.09

1.95

0

Alanine

23.2

32

6.6

22:1 n-9

3.34

2.25

2.5

Arginine

24.7

30.1

9.1

22:6 n-3

5.81

4.96

0.3

Proline

17.3

24

4

20:2 n-6

N/A

N/A

2.2

Tyrosine

13.4

15.6

5

20:4 n-6

N/A

N/A

10.4

a Zhong, Khan, and Shahidi [51]; b Mamelona, Saint-Louis, and Pelletier [52].

4. Bioactive Compounds and Methods of their Extraction and Isolation

Orange-footed sea cucumber is one of the potential marine sources with value-added compounds that could have medicinal properties. The most common bioactive compounds found in C. frondosa are triterpene glycosides, polysaccharides (fucosylated chondroitin sulfate), cerebrosides, saponins, carotenoids, collagens, phenols, PUFA, and other bioactive compounds [5][53][54]. The major bioactive compounds of Atlantic sea cucumber are shown in Figure 3 and explained in the following subsections. This figure does not indicate the location of bioactives, which is shown in the Section 6.
Figure 3. Bioactive compounds of C. frondosa and their potential health benefit.

4.1. Polysaccharides

Over the past few decades, there has been considerable research on marine creatures, and many researchers have focused their attention on polysaccharides derived from marine organisms. Polysaccharides from marine organisms possess potential health benefits, hence are used in food, nutraceuticals, pharmaceuticals, and cosmetic industries. Sea cucumber has ultimately become one of the primary sources of polysaccharides due to its wide range of pharmacological and biological activities. The body walls of C. frondosa contain a high amount of acidic polysaccharides, particularly sulfated polysaccharides (fucosylated chondroitin sulfate) [53][54]. Interestingly, the structure of sulfated polysaccharides identified from sea cucumber is different from other vertebrates, invertebrates, and algae [12]. There are two types of polysaccharides identified in C. frondosa: (a) fucosylated chondroitin sulfate and (b) fucan [54][55]. Fucosylated chondroitin sulfate (FCS) is a unique glycosaminoglycan found in sea cucumber, and its bioactivity depends on the sulfation pattern of monosaccharide composition. Glycosaminoglycans (GAGs) are sulfated, linear, viscous, lubricating, and negatively charged polysaccharides, which are found in mammalian as well as avian species. Bioactivity of FCS depends on the position of sulfate, the degree of sulfation, and the distribution of branches along the backbone. However, chondroitin sulfate (CS) consists of repeating disaccharide unit of glucuronic acid and N- acetylated galactosamine, which is attached by tetrasaccharide linkage with protein cores. CS presents as chondroitin sulfate A (CS-A) which is sulfated at O-4 of N-acetylgalactosamine (GalNAc), CS-C at O-6 position of GalNAc, CS-D at 6 position of GalNAc and glucuronic acid (GlcA), CS-E at 4 and 6 of GalNAc, and CSB which is known as dermatan sulfate (DS) (Figure 4) [56]. Ustyuzhanina et al. [54] isolated fucosylated chondroitin sulfate from the body wall of C. frondosa and found that it comprised of chondroitin sulfate A and E together with the disaccharide repeating units →3)-ẞ-D-GalNAc4S6S-(1→4)-ẞ-D-GlcA3S-(1→ and →3)- ẞ-D-GalNAc4S-(1 → 4)-ẞ-D-GlcA3S-(1→. They also detected three types of branches in C. frondosa; two of them were α-L-Fucp3S4S and α-L-Fucp2S4S link to O-3 of GlcpA residues, whereas the last one was per-O-sulfated α-L-Fucp attached to O-6 of GalpNAc residue. On the other hand, Kale et al. [53] stated that the monosaccharides composition of C. frondosa as N-acetylneuraminic acid, N-acetylgalactosamine, N-acetylglucosamine, glucuronic acid, mannose, fucose, glucose, and galactose.
Figure 4. Structure of repeating disaccharide units in chondroitin sulfate.
The method used to extract the fucosylated chondroitin sulfate (FCS) from sea cucumber includes many steps, such as chemical hydrolysis, proteolytic digestion to release CS, DS, and other GAGs, elimination of proteins and recovery of CS, fractionation of CS, and purification of CS. Chemical hydrolysis and proteolytic digestion can be achieved by using NaOH, cysteine or guanidine HCl, non-ionic detergents, quaternary ammonium salts (cetylpyridinium chloride), urea, potassium thiocyanate or alcoholic solution, whereas recovery of CS can be obtained using trichloroacetic acid. The purification of CS is conducted by using ion exchange, gel filtration, and size exclusion chromatography. The extraction process can be summarized by dilute alkali-enzymatic hydrolysis (alkali solution and papain, trypsin, Alcalase, subtilisin or pepsin), mechanochemically-assisted extraction method, ultrasound-assisted extraction method, organic solvent precipitation, fractionation by precipitation with quaternary ammonium salts and column chromatography [57]. However, many alternative extraction methods have recently been established such as application of high hydrostatic pressure [58], combination of hydrogen peroxide and copper ions [59], tissue autolysis [60], and 60Co irradiation [61], among others.

4.2. Fucoidan

Fucoidan is one of the most important bioactive components of the sea cucumber body walls. This polysaccharide is comprised of L-fucose and sulfate groups. Chain conformation of polysaccharides substantively affects their bioactivities and physicochemical properties [62]. More than 20 species of algae fucoidan have been examined and used in the functional food industries [63]. However, sea cucumber fucoidan has been reported to have antithrombotic and anticoagulant properties [64], inhibition of osteoclastogenesis [65], and protection from gastric damage [66]. Moreover, Wang et al. [67] reported that fucoidan from C. frondosa exhibits anti-hyperglycemic properties, which significantly decreases fasting blood glucose and insulin levels, and increases insulin and glucose tolerance in insulin-resistant mice. Moreover, it has been suggested that C. frondosa fucoidan could be used as a complementary treatment for diet-induced type 2 diabetes. On the other hand, Hu et al. [55] explained that C. frondosa fucoidan significantly prevented high-fat high-sucrose diet injured pancreatic islets, decreased insulin, tumor necrosis factor (TNF)–α, and blood glucose levels, and enhanced adiponectin level. In addition, they proposed that it prevents pancreatic islets apoptosis through inhibition of the mitochondrial pathway. The major extraction method is enzymatic hydrolysis, mainly using papain, followed by cetylpyridinium chloride precipitation [55][67]. The Sepharose Q Fast Flow column is used to purify the crude sulfated polysaccharide.

4.3. Collagen

Collagen, an abundant protein in animals, is mainly spread in the extracellular matrix, inner dermis, tendon, bone, cartilage, ligament, and other connective tissues, which supports an extracellular framework for strength and flexibility [68]. Moreover, 30% of the body protein content is collagen; animal-derived collagen is broadly used in food, pharmaceuticals, and cosmetics industries. Typically, collagen fibers are hardly soluble, and the most common form of collagen is type I (fibrillar collagen) [69]. However, gelatin is a soluble form of collagen, which is obtained by partial hydrolysis of collagen [68]. Due to gel-forming and water-binding properties, gelatin is widely used in food, pharmaceutical, cosmetic, and photography industries as emulsifiers, colloid stabilizers, foaming agents, microencapsulating, and biodegradable film-forming material. Nowadays, the most common raw material for extracting collagen is pigskin (46%), bovine hide (29.4%), pork and cattle bones (23.1%), and aquatic animals at 1.5% [68]. Due to food safety and religious restriction, extraction of collagen from porcine and other mammalian sources is still limited. The potential foot-and-mouth disease of bovine and outbreaks of porcine spongiform encephalopathy have provoked some anxiety among health-conscious consumers [70]. Besides, collagen/gelatin obtained from cows that are not religiously slaughtered and pigs are not acceptable to Muslims and Jews. Collagen from Beef is also prohibited for Hindus [71]. Therefore, marine sources have become a new trend for the extraction of collagen due to being free from such limitations. However, few studies have been researched on extraction of collagen from chicken cartilage, rat tail tendon, kangaroo tail, equine tendon, duck feet, alligators bone and skin, sheepskin, bird feet, frog skin, and some marine sources [72][73].
The most valuable edible part of sea cucumber is the body wall, which represents around 50% of the body weight, mainly considered to consist of collagen and mucopolysaccharides. Collagen is reported to be the major protein of sea cucumber with approximately 70% of insoluble collagen fibrils present in the body wall, while the crude protein in dried sea cucumber estimated around 83% of its dry weight [23][74]. The most abundant type of collagen in sea cucumber is collagen fibrils of echinoderms and type I collagen, which is symmetrically spindle-shaped and short in length [7][75]. C. frondosa has been reported to serve as a good source of thermally stable collagen due to the presence of type I collagen (Figure 5) [76][77]. Moreover, the principal collagen of C. frondosa dermis forms α1 trimers that are covalently linked with the main GAGs found in the dermis. In contrast, it was found that the body wall of C. frondosa contains less than a fraction of one percent collagen. This could be related to the unique feeding habits (mainly phytoplankton, zooplankton, and organic matters) of this species compared to other species (mostly mud or dead particles). Generally, both conventional and novel methods are used for the extraction of collagen from sea cucumber. The conventional methods include chemical hydrolysis (acid and alkali hydrolysis) and enzymatic hydrolysis (trypsin, chymotrypsin, pepsin, papain, bromelain, ficin, proteinase K, collagenase, Neutrase, Alcalase, Protamex or Flavourzyme), whereas novel methods include ultrasound-assisted and pressurized liquid extraction procedures. These newly emerging and novel techniques are considered to offer the best way compared to the conventional methods, due to being safe, economical, time saving, and environmentally-friendly approaches. Lastly, collagen may be purified by using different chromatographic techniques, such as size exclusion chromatography, high-performance liquid chromatography (HPLC), and ion-exchange chromatography.
Figure 5. Primary amino acid sequence of type I collagen.

4.4. Saponins

Saponins are triterpene glycosides and secondary metabolites created by holothurians. They are broadly distributed in plants, animals, and marine organisms (holothurians and sponges) [78]. Saponins play a crucial role in chemical defense as well as pharmacological activities. Approximately 300 triterpene glycosides have been identified and categorized from many species of sea cucumbers, which are named as holostane and nonholostane. Saponins (triterpene glycosides) comprise a carbohydrate chain of up to six monosaccharides, including D-xylose, D-glucose, 3-O-methyl-D-xylose, 3-O-methyl-D-glucose, and D-quinovose. Moreover, about 60% of the triterpene glycosides identified from sea cucumbers have sulfate groups attached to the monosaccharide groups of the carbohydrate chain [79].
The saponin isolated from sea cucumbers, typically known as holothurin, is well known as frondoside A. The C. frondosa species contains various types of triterpene glycosides, mainly frondoside A, frondoside B, frondoside C, isofrondoside C, frondoside A2-1, frondoside A2-2, frondoside A2-3, frondoside A2-4, frondoside A2-6, frondoside A2-7, frondoside A2-8, frondoside A7-1, frondoside A7-2, frondoside A7-3, and frondoside A7-4 (Figure 6) [79][80][81][82][83][84][85][86]. Moreover, C. frondosa comprises a very complex mixture of monosulfated frondoside A, disulfated frondoside B, and trisulfated frondoside C [80][81][82][83][84][85]. Furthermore, Findlay et al. [82] reported that the major saponin in C. frondosa is frondoside A. They also found three novel oligosaccharides, namely frondoside B, frondoside D, and dimeric pentasaccharide frondecaside. Yayli [83] categorized three other minor saponins from C. frondosa, namely frondoside F, frondoside E1, and frondoside E2, though Kalinin et al. [84] stated that the structure of these glycosides and frondecaside is uncertain. These compounds exhibited various biological properties, including cytostatic, hemolytic, antiviral, antiprotozoal, antifungal, anticancer, antineoplastic, and antitumor activities [26][87]. Saponins have been purified by various techniques including liquid-liquid extraction with multiple solvents, high-performance liquid chromatography (HPLC), solid-phase extraction, or chromatography (resins or silica gel). Finally, 1H NMR and 13C NMR spectra are used to identify the structure of the oligosaccharide moiety [83][85].
Figure 6. Chemical structures of different frondosides [79].

4.5. Phenolic Compounds 

Phenolic compounds are powerful antioxidants that are broadly distributed in plants as well as seaweeds, and marine invertebrates. Their effects as beneficial antioxidants to shield the human body from many chronic diseases has been of particular interest. These compounds are partially responsible for flavor, color, bitterness, astringency, and nutritional value of foods [88][89]. Generally, plant-based foods contain around 60 times more antioxidants than their animal-based counterparts. However, sea cucumber, particularly C. frondosa contain a significant amount of phenolics with moderate antioxidant activity even though it is an animal species [16][51][90][91][92]. Due to the absorption of phenolics from phytoplankton, marine invertebrates may possibly serve as a rich source of phenolics including flavonoids, anthocyanidins, anthocyanins, and tannins [51].
It has been reported that the different body parts (muscles, gonads, digestive tract, and respiratory apparatus) of C. frondosa contain a significant amount of phenolics (22.5 to 236.0 mg gallic acid equivalents (GAE)/100 g dw) and flavonoids (2.9 to 59.8 mg of rutin equivalents/ 100 g dw) with oxygen radical absorbance capacity (ORAC) values 140 to 800 µmol of Trolox equivalents/g dw [16]. Moreover, the same study stated that the highest level of phenolics was obtained from the digestive tract using acetonitrile-rich fractions and ethyl acetate extracts, whereas the highest amount of flavonoids was found in the gonads when considering water-rich and acetonitrile-rich fractions. Similarly, Zhong et al. [51] reported that C. frondosa show the highest ORAC (2.60 ± 0.04 mmol of Trolox equivalents/g dw) and 2,2-diphenyl-1-picrylhydrazyl (DPPH) (7.48 ± 0.10 µmol of Trolox equivalents/g dw) activity in rehydrated sea cucumber (mainly internal organs) compared to fresh counterparts, whereas the fresh C. frondosa, with or without internal organs, contained a significant amount of phenolics (1.08 mg GAE/g dw) compared to the rehydrated samples. In another study, Mamelona and Pelletier [93] described that the viscera of C. frondosa exhibited the highest antioxidant activity in ORAC assay in ethanol extracts compared to isopropanol, methanol, and water extracts at 60 °C of extraction by pressure liquid extraction (PLE) method. Additionally, the same study demonstrated that PLE allowed better extraction of α-tocopherol (220 µg/g), total carotenoids (60 mg/g), and total phenols (894 µg/g) by ethanol followed by isopropanol, methanol, and water at 60 °C. In addition, free, esterified, and insoluble-bound phenolics were extracted from different body parts of C. frondosa, and their antioxidant activity was determined. Results suggested that the free fraction was the most predominant form of phenolics in all the selected body parts. Moreover, the highest amount of phenolics and antioxidant property was detected in tentacles (flower), followed by internal organs and body wall [94].
It has been reported that the major phenolic compound in sea cucumbers (Holothuria atra and Holothuria arenicola) is chlorogenic acid (up to 93 wt%), but other phenolics present were pyrogallol, coumaric acid, rutin, and catechin [95].

5. Potential Biological Activities and Medicinal Effects 

Sea cucumber is recognized as a folk medicine and a traditional food globally, particularly in East Asia. However, its specific constituents and their biological functions are yet to be examined. So far, its anti-angiogenic, antithrombotic, anticoagulant, anticancer, antitumor, anti-inflammatory, antihypertension, antifungal, antimicrobial, and antioxidant properties have been investigated. Additionally, it has been used for the treatment of asthma, stomach ulcer, rheumatism, kidney diseases, wound healing, nourishing the body, and as moisturizing agent. Biological and medicinal benefits of C. frondosa are summarized in Table 2.
Table 2. Biologically active compounds of Atlantic sea cucumber and their functions.

Bioactives

Body Parts

Biological and Medicinal Effects

Extraction and Isolation Method

References

Fucosylated chondroitin sulfate

Body wall

Antithrombotic, anticoagulant, anticancer, anti-inflammatory, antitumor, antidiabetic, anti-osteoarthritis, alleviates inflammation, alleviates pain, and improve immune system

Enzymatic (papain/ Alcalase) hydrolysis followed by precipitation (cetylpyridinium chloride/ ethanol/ sodium hydroxide/ tricholoracetic acid)

[54][90][96]

Collagen

Body wall

Antihypertension, antiaging, anti-wrinkle, alleviates skin problems, and wound healing

A divalent cation chelator (EDTA) followed by extraction in water

[76][77]

glycosides (saponins)

Body wall

Antibacterial, antifungal, antiviral, antitumor, anticancer, antiangiogenic, and photo-protective

Isopropyl alcohol/ water extraction and refluxing with

chloroform/ methanol/ethanol

[80][97][98]

Fucoidan

Body wall

Anticoagulant, antibacterial, antiaging, anti-hyperglycemic, lowering blood glucose level, and photo-protective

Hydrolysis with papain and precipitation with cetylpyridinium

chloride

[55][67]

Phenolic compounds

Body wall, tentacles, and viscera

Antioxidants and antibacterial

Solvent extraction (methanol), water, organic solvent (ethyl acetate) and a mixture of water/ miscible organic solvent (acetonitrile)

[16][51]

Cerebrosides

Body wall

Anticancer, anti-inflammatory, and anti-adipogenic activity

Solvent extraction (65% ethanol) and isolated by High-performance liquid chromatography (HPLC), extracted by chloroform/ methanol using high speed counter-current

chromatography

[19][99][100]

Amino acid

Body wall, tentacles, and viscera

Anti-fatigue, repairing tissue, nutritional storage, and wound healing

Reversed phase HPLC

[51][52]

Protein (bioactive peptide)

Body wall

Antimicrobial

Fractionated utilizing ammonium sulfate precipitation and analyzed by size exclusion chromatography

[32]

Vitamin and minerals

Body wall, tentacles, and viscera

Cosmeceutical properties, promote healthy growth and metabolism, lower the blood sugar level

Association of Official Analytical Chemists (AOAC)-and inductively coupled plasma mass spectrometry (ICP-MS)

[52][90]

Omega-3 (EPA)

Body wall, tentacles, and viscera

Anti-hyperglycemic, decrease cholesterol, and protect the heart

Solvent extraction (methanol: chloroform: water) and analyzed by gas chromatography (GC)/ HPLC

[50][51][52][101]

References

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