Bridging the gap between sustainability and profitability: unveiling the untapped potential of sea cucumber viscera

Sea cucumber biology

Sea cucumbers belong to the phylum Echinodermata, along with other marine invertebrates that exhibit radial symmetry (Oh et al., 2017). They are deposit feeders and play a crucial role in coastal mariculture by directly contributing to the recycling of nutrients and the breakdown of detritus and organic matter (Gao et al., 2011; Zamora et al., 2018). Sea cucumbers have numerous shield-like buccal tentacles around the mouth, which are enclosed in the external oral hood (Fig. 3). The body wall of sea cucumbers consists of a thick layer of collagenous connective tissue that envelops and protects their internal organs (Slater & Chen, 2015). Sea cucumbers are found on practically all substrates, including sand, muddy sand, and sandy mud near seagrass, with depths ranging from 1 to 40 m (Lewerissa, Uneputty & Waliulu, 2021; Liubana, Surbakti & Tubo, 2022). They are widely distributed in all oceans (Table S1), inhabiting regions from the Arctic to the tropics, and their habitats vary from the intertidal zone to the deepest seas, such as the bottom of the Mariana Trench (Gonzales-Duran et al., 2021; Liu, Xue & Li, 2022).

Asexual reproduction is possible in sea cucumbers through a process known as fission. They can divide themselves along the median line, where the anterior and posterior ends spin in opposite directions. After a while, the two ends slowly move away from each until they rip the body wall apart, resulting in the division of the organism into two distinct individuals (Al-Rashdi, Eechaut & Claereboudt, 2012). Factors such as failure of sexual reproduction, eutrophication, malnutrition, and environmental stimulation, such as drought during prolonged low tides, can all contribute to the occurrence of asexual reproduction in sea cucumbers (Widianingsih, Hartati & Endrawati, 2014).

In the wild, sea cucumbers naturally gather in groups consisting of more than ten individuals spaced approximately 5 m apart to perform simultaneous spawning. This synchronized behaviour ensures the highest possible fertilization rates during sexual reproduction (Rahman & Yusoff, 2017). Sea cucumber eggs are externally fertilized when the male and female gametes fuse in the water column, as shown in Fig. 4. Fertilized eggs quickly progress to the blastula stage within an hour after fertilization, and by the end of the day, they reach the typical gastrula stage. After two days, the fertilized eggs transform into planktonic auricularia larvae, which exhibit a pelagic habit and feed on suspended microalgae (Kumara et al., 2013). After approximately two weeks, sea cucumber larvae will reach the doliolaria stage (non-feeding stage). From there, they metamorphose into the pentactula stage and subsequently into early juveniles. At this stage, they begin to feed by grazing on the biological film covering the leaf surface. As they grow and mature into adults over another week or two, then move down into the sediment and begin grazing in deeper areas (Altamirano & Rodriguez, 2022).

The reproductive success of sea cucumbers relies on their social behaviour, population diversity and density, chemical communication, and egg-laying synchronization (Scannella et al., 2022). A reduction in population density can have an impact on fertilization and lead to a decrease in population size, thus affecting their reproductive success (Hasan, 2019; Gonzales-Duran et al., 2021). Holothurians are vulnerable to changes in pH, temperature, and salinity (Liu, 2015; Gonzales-Duran et al., 2021), which can impact their population frequency, growth, and survival rates (Kashenko, 2000; Dong et al., 2011; Liu, 2015; Zhou, Zhang & Li, 2018). Additionally, larval development and survival are highly susceptible to climate change (Asha & Muthiah, 2005; Zamora & Jeffs, 2013; Liu, 2015; Gonzales-Duran et al., 2021). Fluctuations in these environmental variables trigger a variety of biochemical and physiological adaptations that delay larval metamorphosis, especially during the gastrulation stage, which marks the development of digestive tract feeding activity. This results in slower larval development, increases the risk of predation, and adversely affects larval survival (Asha & Muthiah, 2005; Gonzales-Duran et al., 2021).

Nutritional value of sea cucumber

The consumption of sea cucumbers as food products, tonics and aphrodisiacs is only popular in China and other Asian countries (Han, Keesing & Liu, 2016). However, sea cucumbers are very nutritious, and the bioactive components found in them are valuable for both the food and the biomedical industries (Pangestuti & Arifin, 2018). The body wall is the main part of the sea cucumber that is consumed and consists mainly of epithelial and dermal connective tissues, collagenous fibres, proteoglycans, glycoproteins, and amorphous interstitial materials (Yang, Hamel & Mercier, 2015).

The proximate compositions (moisture, protein, lipid, ash, and carbohydrates) of various sea cucumber species are shown in Table 1. Most sea cucumber species exhibit high amounts of saturated fatty acids (SFAs) and monounsaturated fatty acids (MUFAs) (Table 2) and are abundant in essential amino acids (Table 3). SFAs were found to be the dominat fatty acid elements in H. scabra (71.76%), H. leucospilota (69.57%), and H. atra (57.04%) (Ridzwan et al., 2014).

Additionally, sea cucumbers have outstanding vitamin and mineral profiles, including vitamins A (455 µg/100 g), B1 (thiamine) (0.04 mg/kg), B2 (riboflavin) (0.06 mg/kg), B3 (niacin) (0.4 mg/kg), C (3.19 mg/100 g), and E (2.82 mg/100 g), as well as essential minerals, particularly calcium, magnesium, and iron (Bordbar, Anwar & Saari, 2011; Sroyraya et al., 2017; Achmad et al., 2020; Ardiansyah et al., 2020) (Table 4). Notably, Stichopus vastus had the highest mineral content compared to other species. In addition to being valuable marine commodities, sea cucumbers are a significant source of medicine (Zhao et al., 2018). They are used in traditional Chinese medicine and are thought to have therapeutic capabilities, to treat conditions such as arthritis, high blood pressure, asthma, cancer, frequent urination, and impotence (Guo et al., 2015; Pangestuti & Arifin, 2018; Liang et al., 2022). They have extensive uses in the biomedical industry, where they are believed to possess therapeutic capabilities (Zohdi et al., 2011) and numerous active ingredients, including polysaccharides, peptides, proteins, lipids, (Janakiram, Mohammed & Rao, 2015), collagen, gelatine, saponins and acid mucopolysaccharides (Kariya et al., 2004; Lu et al., 2010; Zhou, Wang & Jiang, 2012; Yang, Hamel & Mercier, 2015).

Socio-economic status of sea cucumber

Monetized marine resources, such as sea cucumbers, greatly support the livelihoods of coastal communities in the Indo-Pacific region (Hair et al., 2019). Sea cucumbers are easily processed (gutted, boiled, and dried) using basic, affordable tools (Ram et al., 2017; Hair et al., 2019). They are relatively sedentary, making them easy to collect (Wolfe & Byrne, 2022). They are commonly harvested by fisher in traditional ways, such as collecting from coral reefs at low tide or by diving in shallow waters (Friedman et al., 2008; Plaganyi et al., 2020; Prasada, 2020).

Coastal communities process sea cucumbers and sell the final products at a higher price. The processed and dried body wall of sea cucumbers, known as ‘beche-de-mer’, is a valuable marine export commodity and an important source of income for coastal communities. It is massively exported throughout Asia and is highly regarded as a seafood delicacy. Prices for sea cucumbers can fetch up to US$983.47 per kilogram in China or US$110.78 per kilogram in Japan (Kinch et al., 2007; Purcell, Williamson & Ngaluafe, 2018; Hair et al., 2019; Wolfe & Byrne, 2022). The market price on the market is not only based on the type and species but also on size. There are various grades of processed sea cucumbers in demand, but in general, sellers often grade sea cucumbers into at least three grades: grade 1 (largest size), grade 2 (medium size) and grade 3 (smallest size) (Ochiewo et al., 2010).

Greater quantities of ‘beche-de-mer’ are exported to Asia, where it is a valuable product. Louw & Burgener (2020) reported Madagascar is the top exporter of dried sea cucumbers, sending 40% of its total exports to Asian markets between 2012 and 2019. Hong Kong serves as a major importer and commercial hub for dried seafood, including sea cucumber (Ben-Hasan et al., 2021). Over the past 8 years, Hong Kong has been the greatest importer in Asia, bringing in almost 56 million kg from around the world. However, nearly 70% of its total imports are then re-exported to mainland China (Jun, 2009; Louw & Burgener, 2020; Ben-Hasan et al., 2021). Due to the high demand in the Asian market and the high shipping costs that restrict reef fish exports, sea cucumber fisheries have become the second-most profitable export fishery in the South Pacific, after tuna (Carleton et al., 2013).

Novel sulphated polysaccharide

The viscera of sea cucumbers are a good source of nutrients. The purified chondroitin sulphate polysaccharides from the digestive tract of Apostichopus japonicus are postulated to have anti-tumour proliferation properties (Wei, Jian & Mao, 2011; Xin, Jing & Jian, 2016), whereas the purified sulphated polysaccharides from Pattalus mollis have an anticoagulant effect (Zheng et al., 2019). Sea cucumber viscera contain approximately4.9% crude polysaccharides, from which sulphated polysaccharides can be extracted (Yang et al., 2020). Sulphated polysaccharides have a variety of beneficial biological properties, including anticoagulant, antiviral, antioxidant, anticancer, and immuno-inflammatory properties, making them suitable for nutraceutical, cosmeceutical, and pharmaceutical applications (Wijesekara, Pangestuti & Kim, 2011; Jiao et al., 2011; Zhu et al., 2018).

Novel saponins

Sea cucumber viscera are abundant in saponins—secondary metabolites that influence metabolism and enhance the immune system by reducing cholesterol and exhibiting anti-cancer (Shi et al., 2004) and anti-bacterial properties (Sumarto & Karnila, 2022). Recent studies revealed that viscera contain higher saponin content than their body walls (Zhang et al., 2018). Novel saponins with potent fungicidal, antioxidant, anti-viral, and anti-cancer effects have been identified and purified from the viscera of Holothuria scabra, Holothuria lessoni and Apostichopus japonicus, making them promising candidates for cosmeceutical, medical, and pharmaceutical applications (Bahrami, Zhang & Franco, 2014; Zhang et al., 2018; Sumarto & Karnila, 2022).

Novel source of nutrients

Numerous nutrients, including oligosaccharides, phenols, flavonoids, and trace metals, have been found in the viscera of sea cucumbers (Zhang & Chang, 2014). the reported proximate composition of sea cucumber viscera may differ among studies (Table 1) due to species, sample preparation techniques, feed, and environmental factors such as habitat and climate. Sea cucumber viscera contain low lipid but high protein contents. He et al. (2017) demonstrated that protein hydrolysate from sea cucumber viscera had high antifatigue and antioxidant activity. Additionally, due to their high profile of essential amino acids, sea cucumber protein hydrolysate may be a suitable dietary protein source (Senadheera, Dave & Shahidi, 2021).

Babji et al. (2020) reported that sea cucumber viscera contain high levels of vitamins. The consumption of a relatively small amount of sea cucumber viscera may satisfy the nutritional needs for several vitamins such as vitamins A, B, C, and E in both animal and human diets, which support the immune system, strengthen bones, heal wounds, turn food into energy, and repair cellular damage. The vitamin content in sea cucumber viscera is shown in Table 5. According to Table 5, vitamin B3 (nicotinic acid) is the most abundant vitamin in the viscera of both C. frondosa (Mamelona, Louis & Pelletier, 2010) and undetermined species (Babji et al., 2020).

Furthermore, sea cucumber viscera contain a significant number of essential minerals (e.g., Cu, Fe, Zn, K, Na, Mn, As, Mg, Se, Ni, and Ca) that play important roles in maintaining general biological systems, along with relatively small amounts of nonessential trace elements (Cd, Co, and Pb) (Mamelona, Louis & Pelletier, 2010). The mineral composition of sea cucumber viscera is shown in Table 4. Babji et al. (2020) reported that sodium is the highest element content in sea cucumber viscera, approximately 338.3 g/100 g, while potassium was found to be the most abundant element in Cucumaria frondosa, at approximately 1.870 g/100 g, as reported by Mamelona, Louis & Pelletier (2010), and 0.200 g/100 g, as reported by Ramalho et al. (2020). Potassium is a micromineral that regulates the activity of blood cells and muscles, especially the heart muscle, maintains fluid balance in the body, regulates blood pressure, and acts as an enzyme activator (Susanti, Sukmawardani & Musfiroh, 2016).

Sea cucumber viscera are rich in fatty acids, especially eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), which are essential micronutrients with beneficial health impacts (Shepon et al., 2022). In addition, Mamelona, Louis & Pelletier (2010) reported that sea cucumber viscera are abundant in essential amino acids, which play a crucial role in metabolic pathway regulation and are crucial components in growth, development, and reproduction. The fatty acid and amino acid profiles of sea cucumber viscera reported by several studies are shown in Tables 2 and 3, respectively. Liu et al. (2021) highlighted that EPA was the predominant fatty acid, constituting 27.76% of the total fatty acids found in the viscera of Cucumaria frondosa. This percentage is significantly higher than that of crude oil from other marine byproducts, which typically contain only 4.63–9.54% EPA. EPA, as an essential omega-3 fatty acid, has been linked to numerous positive health effects, including decreased cardiovascular risk, stimulation of foetal development, and improved cognitive function (Swanson, Block & Mousa, 2012). Therefore, sea cucumber viscera can be valorised to produce omega-3 PUFAs (especially EPA) and EPA-enriched nutritional products. Additionally, approximately 25.93% (Liu et al., 2021) and 14.30% (Mamelona, Louis & Pelletier, 2010) of the total amino acids in the viscera of Cucumaria frondosa are composed of glutamine, which is essential for cellular metabolic activities and animal immunity (Binod et al., 2017; Shah, Wang & Ma, 2020). The nutritional content of sea cucumber viscera and the richness of their metabolites indicates their enormous potential for being transformed into high-value products.

Due to their high nutritional value sea cucumber viscera have traditionally been consumed both raw and processed in some countries. In Samoa, Stichopus horrens is the most sought-after species, as the viscera are consumed raw and commercially sold in local markets, while the body parts are returned to the sea alive (Eriksson et al., 2007; Charan-Dixon et al., 2019). In addition, salt-fermented sea cucumber viscera, known as konowata, is one of the three major Japanese delicacies that are commercially consumed in Japan (Nishanthan et al., 2021). Their edibility and nutritional value indicate their potential to be consumed as therapeutic foods.

Valorisation of sea cucumber viscera into value-added products

Sea cucumber viscera contain sulphated polysaccharides (e.g., sulphate, fucose, galactosamine) that can be used in pharmacological activities, such as improving gut health, antiviral mechanisms and wound healing (Cao, Surayot & You, 2017; Li et al., 2021). Conventional extraction methods, such as chemical methods can be applied to extract sulphated polysaccharides from sea cucumber viscera. However, the alkaline conditions during the chemical extraction process can influence the conformation of sulphated polysaccharides, leading to potential degradation and desulphation of the polysaccharides. Consequently, this may affect the physicochemical and biological properties of the polysaccharides (Li et al., 2021).

Due to the limitations of conventional extraction methods, microwave-assisted extraction has emerged as a promising technology to minimize degradation and desulphation during the extraction of sulphated polysaccharides from sea cucumber viscera. The use of microwave heating can lead to a reduction in the use of solvents, thereby lowering operating costs. Moreover, microwave radiation provides rapid heating, which, in turn, reduces energy consumption during extraction (Wan Mahari et al., 2022). The microwave radiation generated during heat activation can contribute to cell wall lysis and break the protein bonds to release the cellular contents and polysaccharides into the extraction medium. However, further studies are needed to optimize the operating conditions (e.g., microwave power, duration) during microwave-assisted extraction to enhance the yield and properties of sulphated polysaccharides.

Enzymatic hydrolysis is another emerging technology that can be applied to improve the extraction of sulphated polysaccharides (Wang et al., 2022). The types of proteases (e.g., papain, pancreatin) and duration of hydrolysis are important factors that influence the release of polysaccharides from sea cucumber viscera and their biological properties. Previous study reported that protein hydrolysates produced by pancreatin exhibited greater antioxidant activity compared to that produced by papain (Karamac, Kosińska-Cagnazzo & Kulczyk, 2016). Therefore, further studies should be scrutinized to develop an extraction method that can enhance the production of sulfated polysaccharides with desirable physicochemical and biological properties.

Potential cosmetic ingredients from sea cucumber viscera

The abundance of essential active compounds found in sea cucumber viscera extracts highlights their high potential for use in the cosmeceutical field. Studies have reported that sea cucumber (S. japonicus) viscera extracts promote the expression of tyrosinase, tyrosinase-related protein (TRP-1 and TRP-2), and microphthalmia-associated transcription factor (MITF) protein levels, as well as extracellular-regulated kinase (ERK) activation. These elements are known to be effective in skin whitening and anti-ageing treatments by reducing melanin production and increasing collagen synthesis through ERK signalling (Kwon et al., 2018).

Potential as animal nutrition supplements and feed additives

In aquaculture, good nutrition is essential for the optimal growth and production of high-quality products, and the feed component typically represents approximately 60–80% of the production cost (Ragasa, Osei-Mensah & Amewu, 2022). Feed additives are products used to enhance nutrients and reduce production costs. Functional feed additives in animal food stimulate growth, promote good health, boost the immune system, and provide physiological advantages over conventional feeds (Alemayehu, Geremew & Getahun, 2018).

Sea cucumber viscera are a high-value source of nutrients and bioactive compounds that can be used as functional feed additives in the aquaculture industry. Babji et al. (2020) successfully converted sea cucumber viscera into prospective health supplement products for the agro-based food and health industries using an enzymatic hydrolysis method. This review demonstrates the potential of turning waste materials into high-value products, which not only increases the market value of sea cucumber viscera but also helps reduce waste that could otherwise pollute the environment.

Potential as sex reversal agent for aquatic animal

The males of many species of ornamental fish have highly pigmented bodies and usually more developed fins, making them preferred over female fish by hobbyists (Piferrer & Lim, 1997). Due to the higher demand for these male fish, the use of sex reversal technology for commercial production of an all-male population of these aquatic animals could significantly increase the economic benefits of this type of aquaculture operation. The hormones used for sex reversal to produce all-male fish are testosterone, 17-α-methyltestosterone, and androstenedione. In aquaculture, sex reversal can be triggered by using steroid hormones either through immersion, injection, or oral administration by feeding. However, synthetic steroids have a negative impact on the environment and the fish itself (Emilda, 2015). Therefore, it is essential to explore natural steroid sources that are safe for both humans and the environment.

Testosterone, the steroid hormone used in sex reversal, is naturally produced in sea cucumbers. The potential utilization of sea cucumber extract as a natural source of testosterone is promising. However, the optimal extraction method has yet to be determined. Recently, studies have been conducted on sex reversal in aquatic animals using steroid extracts from sea cucumber viscera. Emilda (2015) and Saputra et al. (2018) reported that using the immersion technique to administer steroid extracts from sea cucumber viscera can enhance the percentage of male guppies by 65.13% and 88.9%, respectively. Riani, Sudrajat & Triajie (2010) reported that injecting testosterone hormone from sea cucumber viscera into giant freshwater prawns can produce 63.33% male prawns. The hormone is also effective in influencing zygotes and larvae to develop into male prawns without negatively impacting motility, fecundity, and hatching rates. This research provides crucial baseline information, indicating that sea cucumber viscera can serve as a natural steroid source for sex reversal in aquatic organisms.

Promising neuroprotective agent in debilitating central nervous system disorders

Triterpene glycoside or saponins are natural bioactive compounds found in sea cucumbers (Bahrami, Zhang & Franco, 2018). Numerous studies have demonstrated that the medicinal and health benefits of sea cucumbers are attributed to the presence of saponins, which are the most significant and primary secondary metabolites found in sea cucumbers (Zhao et al., 2018). Saponins have neuroprotective properties against a number of central nervous system disorders (Mitu et al., 2017).

Kleawyothatis et al. (2022) reported that the whole body (including viscera) and body wall extracts of sea cucumber (H. scabra) contain triterpene glycosides or saponins. These extracts have been shown to provide a neuroprotective effect against central nervous system disorders, specifically Alzheimer, in Caenorhabditis elegans models. The observed decrease in amyloid-β deposition and aggregation, along with the reduction in reactive oxygen species, resulted in lifespan extension of C. elegans Alzheimer’s disease models. These findings strongly suggest that sea cucumber extracts possess natural preventive and therapeutic properties for Alzheimer’s disease. Meanwhile, Bahrami, Zhang & Franco (2018) mentioned that sea cucumber viscera had substantially greater relative levels of saponins than the body and also contained some saponin congners. Although saponins are known to have significant neuroprotective properties (Mitu et al., 2017), further studies are needed to validate the role of saponins found in sea cucumber viscera in preventing and treating debilitating central nervous system disorders.