Introduction

Sea cucumber is one of the most potential export commodities from marine sectors in Indonesia. Sea cucumber commercially traded either in fresh or dehydrated form. It categorized based on economic value (low, medium or high) depends on several aspects such as species, appearance, abundance, color, odor, body wall thickness, market trends and needs¹. It is well known as functional food due to its functional properties and have been consumed in Asian country for centuries². However, this potential may lead to over exploited which may result in a population collapse.

Sea cucumber are abundant in tropical region like Indonesia. Total catching of sea cucumbers in the world has reached 100,000 tons annually. According to the Food and Agriculture Organization’s (FAO) global statistics reports in 2004, Indonesia has been the world’s largest producer of sea cucumbers based on global reports of major importing countries, Hongkong and China. In addition, Indonesia still one of the major sea cucumber fisheries till now ^2,4,5.

One of the high-value sea cucumbers comes from Holothurian species with total 1200 species recorded all over the world (Mc Elroy, 1990). H. nobilis (black teatfish), H. fuscogilva (white teatfish), and H. scabra (sandfish) commonly trade in Indonesia. They are generally distributed in tropical waters in the Western Pacific and the Indian Ocean^6,7. Holothuroidea are rich in functional materials, including saponin, chondroitin sulfate, collagen, amino acids, and phenols⁸. This bioactive material will lead to potential development not only in food industries but also biomedicine industries⁹.

Figure 1: Holothuria Scabra from Bungin Island Click here to View Figure

Utilization of sea cucumbers in Indonesia as food compared with other fishery products are low and less popular, because sea cucumbers have a low aesthetic value seen from the physical form. However, sea cucumbers have a high nutritional content. The purpose of this research is to present the nutritional value and heavy metals content of sea cucumber H. scabra from 4 different locations that has potential  source of functional food in the future.

Material and Methods

Sample Collection and Preparatio

H. scabra samples used in the present work were fresh sea cucumber collected from four different coastal areas in Indonesia including Bungin Island (West Nusa Tenggara) S 06^o24.103’ E 116^o04.707’ collected on 2017, Belitung Island S 02^o32.239’  E 107^o37.217’, Lampung S 05^o33.706’  E 105^o16.220’ and Makassar S 05^o27.114’  E 119^o23.822’ collected on 2018. The samples were instantly dissected to remove viscera, cleaned, packed with ice prior sending to the laboratory and kept in dark container at -80°C until analyze.

Proximate Analysis 

Proximate compositions of H. scabra were analyzed as follows. The moisture, ash and protein were determined according to the standard AOAC method⁸. In brief, the samples were air-dried in an oven at 100°C for 18 hours then cooled in a desiccator and weighed. Weight lost was reported as moisture content. Ash content was analyzed by incineration in a muffle furnace at 550°C for 24 hours. Lipid content was measured by conventional soxhlet extraction using hexane solvent for 24 hours and carbohydrates were calculated by difference.

Vitamins, Minerals and Heavy Metals Analysis

Vitamin A and E content were analyzed using HPLC Alliance Waters, Photo Diode Array (PDA) with LiChrospher 100 RP-18 (5um) 4 mm x 250 mm column while vitamin B₁ B₂, and B₁₂ content were determined by using UPLC H Class Waters, Photo Diode Array (PDA) with ACQUITY UPLC BEH Amide 1.7 um 2.1 x 100 mm column. Minerals content including calcium (Ca), potassium (K), iron (Fe), and sodium (Na) were analyzed by the standard AOAC method¹⁰ while the phosphorus (P) content was analyzed by spectrophotometric method. The heavy metals content including mercury (Hg), lead (Pb), cadmium (Cd), and arsenic (As) were analyzed by the standard AOAC method¹¹.

Amino Acid Composition

Amino acid profile was analyzed with UPLC apparatus with condition: Mobile phase (Gradient composition system); Flow rate (0.5 ml per minute); Injection volume (1 μL). Column used (AccQ.Tag Ultra C18 1.7 μm (2.1 x 100 mm), Waters); Detector (PDA, wavelength 260 nm); and Temperature (49^oC).

Fatty Acid Composition

Determination of fatty acid was analyzed by gas chromatography (GC) with condition: Flow rate (18.0 cm/sec with column length 100 m); Injector temperature (225ºC), ;Column (Supelco SPTM 2560 100m 0.25 mm 0.2 μm); Carrier Gas (N₂), Detector FID (240ºC); and Split (1:100).

Results

Nutrient composition of H. scabra collected from four different locations is depicted in Table 1. Table 2. shows the heavy metal contents of all H. scabra samples. The amino acid and fatty acid compositions were given in Table 3 and 4.

Table 1: Nutrient Content of Sea Cucumber Holothuria Scabra

Note. Numbers in parentheses are standard deviations. Means sharing subscripts differ at p < 0.05 according to Duncan Significant Difference comparison. *nd=not detected

Table 2: Heavy Metal Content of Sea Cucumber Holothuria Scabra

Note. *nd=not detected

Table 3: Amino Acid Composition Of Sea Cucumber Holothuria Scabra

Note. Numbers in parentheses are standard deviations. Means sharing subscripts differ at p < 0.05 according to Duncan Significant Difference comparison. *nd=not detected

Table 4: Fatty Acid Composition of Sea Cucumber Holothuria Scabra

Note. Numbers in parentheses are standard deviations. Means sharing subscripts differ at p < 0.05 according to Duncan Significant Difference comparison. *nd=not detected

Discussion

It has been reported that sea cucumbers are also a source of vitamins and minerals. In our work, all H. scabra samples were checked for their vitamin contents including vitamin A, B₁, B₂, B₁₂ and E. Similarly to previous research, vitamin E was detected in the H. scabra yet vitamin A was not detected¹⁴. Meanwhile, sodium (Na) was the second largest mineral content followed by magnesium (Mg), potassium (K), phosphorus (P), iron (Fe). According to Diniz et al. (2012), the chemical composition of marine organisms, in general, may be influenced by a number of factors such as physiological characteristics, environmental conditions, habitat and life cycle¹⁸.

All heavy metals were analyzed in this study (Table 2) including Hg, Pb, Cd and As were not detected. Total 18 amino acids were identified (Table 3), 7 of them including Threonine, Leucine, Lysine, Valine, Isoleucine, Phenylalanine, and Methionine are essential amino acid needed for human. Glycine, proline and glutamic acid were the most abundant constituent in the sea cucumber H. scabra. In the case of fatty acids (Table 4), omega-6 from Bungin Island and Makassar were the major constituent in this species with 0.1834 % and 0.1377%. Meanwhile, omega-9 from Belitung Island and Lampung were the major constituent in this species with 0.2466 % and 0.1773 %. Eicosapentanoic acid (EPA) detected in all sampling locations but Docosahexaenoic acid (DHA) only found in Belitung Island and Makassar.

The heavy metals content in sea cucumber is specific, depend on sampling location and body compartment¹⁹. All the non-essential metals in the body wall of this H. scabra was below the allowed limits for human consumption as recommended by Indonesia, the US; Australia; the UK and European^20-23. It means that H. scabra safely to consume.

Glycine, proline and glutamic acid were the most abundant constituent in the sea cucumber H. scabra. It is in line with another journal that said a high amount of proline was found in H. scabra only¹⁴. Arginine and tyrosine as semi-essential amino acid also detected nevertheless Histidine, Cysteine, Tryptophan were not detected.

Previous study conclude that a sea cucumber is a healthy food for human to reduce hypercholesterolemia due to ratio of lysine to arginine. According to this result the composition of lysine to arginine was good compared with another sea cucumber species such as A. japanicus (0.62)²⁴.

Omega-6 fatty acids have the potential to influence a number of chronic disease, such as cardiovascular disease and atherosclerosis²⁵. On the other hand omega-3 found in this result was 0.0572 %. Omega-3 fatty acids including eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), are found naturally in fish oil and have the potential to be anti-inflammatory nutrient. It has been studying that it took role for the treatment of allergic diseases, arthritic pain, neuropatic pain, hypertriglyceridemia and cardiovascular prevention^26-29. EPA and DHA are synthesized by marine plants both unicellular and multicellular such as phytoplankton and algae. They are eventually transferred through the food web and are incorporated into lipids of aquatic species³⁰. The present results find that EPA detected in all sampling locations but DHA only found in Belitung Island and Makassar. It might be because of as a result of diet factors.

Previous study by Ridzwan et al¹⁵ reported that saturated fatty acids in H. scabra were found dominated compared with unsaturated fatty acids. In this study, it happened only in Bungin Island. Another locations showed that unsaturated fatty acids were higher than saturated fatty acids. Main fatty acid found in the whole body were Palmitic acid, Oleic acid, Linoleic acid (LA), and Arachidonat acid (AA). There are also Alfa Linolenic acid (ALA), precursor fatty acid of the omega-3 fatty acids and Arachidonic acid (AA) as essential fatty acid for human, found in H. scabra in Bungin Island and Belitung Island. ALA is the precursor for longer chain unsaturated omega-3 to a limited extent desaturated to EPA and DHA. Through enzymatic metabolism of LA and ALA also generates arachidonic acid.

Conclusion

The high protein value and low fat were found in the sea cucumber Holothuria scabra from all sampling locations. The major mineral content were Calcium, Sodium, and Magnesium. Glycine was the major component of amino acid. Omega-6 and omega-9 were the major component of fatty acid. All heavy metals analyzed in this study were not detected. It can be inferred that the sea cucumber H. scabra is safely to consume and can be used as functional food in the future.

Funding Sources

Ministry of Research, Technology and Higher Education of the Republic of Indonesia

Conflict of Interest

The authors have no potential competing interests.

Acknowledgment

We would like to extend special gratitude to Ministry of Research, Technology and Higher Education of the Republic of Indonesia for supporting this research by INSINAS grant program.

References

1. Abdulrazaq M., Innes J. K., Calder P. C. The effect of omega-3 polyunsaturated fatty Wen J., Hu C., and Fan S. Chemical composition and nutritional quality of sea cucumbers. Sci. Food Agric. 2010; 90:2469–2474.
   CrossRef.
2. Torai-Granada V., A. Lovatelli, and M. Vasconcellos. FAO Fisheries and Aquaculture Technical Paper No. 516. Food and Agriculture Organization of the United Nations, Rome, Italy. 2008; 257-282.
3. Perez-Espadas A. R., Verde-Star M. J., Rivas-Morates C., Oranday-Cardenas A., Morales-Rubio M. E., Leon-Deniz L. V., Canul-Canche J., and Quijano L. In vitro cytotoxic activity of Isostichopus badionotus, a sea cucumber from Yucatan Peninsula coast. Journal of Pharmacy and Nutrition Sciences. 2014; 4: 183-186.
   CrossRef.
4. Choo P. Population status, fisheries and trade of sea cucumbers in Asia. In: V.Toral-Granda., A. Lovatelli and M. Vasconcellos (eds). Sea cucumbers: A global review of fisheries and trade. FAO Fisheries and Aquaculture Technical Paper No. 516. Food and Agriculture Organization of the United Nations, Rome, Italy. 2008; 81–118.
5. Haider M. S., Sultana R., Jamil K., Lakht-e-Zehra, Tarar O. M., Shirin K., and Afzal W. A study on proximate composition, amino ac Id profile, fatty acid profile, and some mineral contents in two species of sea cucumber. The Journal of Animal & Plant Sciences. 2015; 25(1): 168-175.
6. Preston, Garry L. Bech-de-mer. In: Wright, A & Hill, L (Eds), Nearshore Marine Resources oh the South Pasific. International Centre for Ocean Development, Canada, 1993: 371-407.
7. Conand, C. Population status, fisheries and trade of sea cucumbers in Africa and the Indian Ocean. In V. Toral-Granda, A. Lovatelli and M. Vasconcellos (Eds). Sea cucumbers. A global review of fisheries and trade. FAO Fisheries and Aquaculture Technical Paper. No. 516. Rome, FAO. 2008; 143–193.
8. Siahaan E. A., Pangestuti R., Munandar H., and Kim S. K. Cosmeceuticals Properties of Sea Cucumbers: Prospects and Trends. MDPI / Cosmetics. 2017; 4(3): 26
   CrossRef.
9. Pangestuti R., Arifin Z. Medicinal and health benefit effects of functional sea cucumbers. Journal of Traditional and Complementary Medicine. 2018; 8(3): 341–351.
   CrossRef.
10. Official Methods of Analysis of the Association of Official Analytical Chemists, 15^th ed. Washington D.C. 1990.
11. Official Methods of Analysis of the Association of Official Analysis Chemists, 17^th ed. Washington D.C. 2000.
12. Azad S. A., Shaleh S. R. M., Siddiquee S. Comparison of fatty acid and proximate composition between Holothuria edulis and Holothuria scabra collected from coastal water of Sabah, Malaysia. Advances in Bioscience and biotechnology. 2017; 8: 91-103.
    CrossRef.
13. Smiley S. Holothuroidea. Microscopic Anatomy of Invertebrates.1994;14: 401-471.
14. Sroyraya M., Hanna P.J., Siangeham T., Tinikul B., Jatiujan P., Poomtong T., and Sobhon P. Nutritional components of the sea cucumber Holothuria scabra. Functional Food in Health and Disease. 2017; 7(3): 168-181.
    CrossRef.
15. Ridzwan B. H., Hanita M. H., Nurzafirah M., Norshuhadaa M. P. S., Hanis Z. F. Free Fatty Acids Composition in Lipid Extracts of Several Sea Cucumbers Species from Malaysia.  International Journal of Biosciences, Biochemistry and Bioinformatics. 2014; 4(3): 204–
    CrossRef.
16. Ibrahim, M. Y., Elamin, S. M., Gideiri, Y. B., Ali, S. M. The proximate composition and the nutritional value of some sea cucumber species inhabiting the sudanese red sea. Food Science and Quality Management. 2015; 41: 11–
17. Wang J. F., Gao S., Wang Y. M., Ma Q., Ren B. X., Xue C. H. Effects of Isostichopus fuscus on the Lipid Metabolism in Hipercholesteremic Rats. Periodical of Ocean University of China. 2009; 39:228–232.
18. Diniz G. S., Barbarino E., Lourenço S. O. On the Chemical Profile of Marine Organisms from Coastal Subtropical Environments: Gross Composition and Nitrogen-to-Protein Conversion Factors. Oceanography. 2012; 297-320.
19. Mohammadizadeh M., Esmaeilzedah M. Heavy metal accumulation in tissues of two sea cucumbers, Holothuria leucospilota and Holothuria scabra in the northern part of Qeshm Island, Persian Gulf. Marine Pollution Bulletin. 2016; 354-359.
    CrossRef.
20. National Standardization Agency of Maximum contamination limit of
    heavy metals in food SNI 7387-2009. Indonesia. 2009.
21. S. Department of Health and Human Services, Public Health Service, Food and Drug Administration. Guide for the control of molluscan shellfish. National Shellfish Sanitation Program. 2003.
22. Otway N. M. Bioaccumulation studies on fish: choice of species, sampling, designs, problems and implications for environmental management. In: Miskiewicz, A.G. (Ed.), Assessment of the Distribution, Impacts and Bioaccumulation of Contaminants in Aquatic Environments Proceedings of a Bioaccumulation Workshop. Water Board and Australian Marine Sciences Association Inc., Sydney, 1992; 103–113.
23. Tyrrell L., Mchugh B., Glynn D., Twomey M., Ioyce E., Costello J., Mcgovern E. Trace metal concentrations in various fish species landed at selected Irish ports. Mar. Environ. Health Ser. 2005; 20: 1–19.
24. Yang H., Hamel J. F., Mercier A. The sea cucumber Apostichopus japonicus: history, biology and aquaculture. Academic Press. 2015; 39:1-478.
25. Mori T. A. and Hodgson J. M. Fatty Acids: Health Effects of Omega-6 Polyunsaturated Fatty Acids. Elsevier, Encyclopedia of Human Nutrition. 2013; 2: 209-214.
    CrossRef.
26. Miyata J., and Arita M. Role of omega-3 fatty acids and their metabolites in asthma and allergic diseases. Allergol Int. 2015; 64(1): 27–34.
    CrossRef.
27. Abdulrazaq M., Innes J. K., Calder P. C. The effect of omega-3 polyunsaturated fatty acids on arthritic pain: A systematic review. Nutrition Journal. 2017; 39–40: 57-66.
    CrossRef.
    
28. Arca M., Borghi C., Pontremoli R., DeFerrari G. M., Colivicchi F., Desideri G., Temporelli P.L. Hypertriglyceridemia and omega-3 fatty acids: their often overlooked role in cardiovascular disease prevention. Nutr Metab Cardiovasc Dis. 2018; 28(3):197-205.
    CrossRef.
    
29. Trevor A. Mori, Marine OMEGA-3 fatty acids in the prevention of cardiovascular disease. Fitoterapia. 2017; 123: 51-58.
    CrossRef.
    
30. Shahidi F. and Ambigaipalan P. Novel functional food ingredients from Marine Sources. Current Opinion in Food Science. 2015; 2: 123–129
    CrossRef.