chemical composition and nutritional quality of sea cucumbers

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Research ArticleReceived: 5 May 2010 Accepted: 29 June 2010 Published online in Wiley Online Library: 17 August 2010

(wileyonlinelibrary.com) DOI 10.1002/jsfa.4108

Chemical composition and nutritional qualityof sea cucumbersJing Wen,a,b Chaoqun Hua∗ and Sigang Fana

Abstract

BACKGROUND: The dried form of sea cucumbers has been a seafood and medicinal cure for Asians over many centuries. In thisstudy the chemical composition and nutritional quality of eight common sea cucumbers (Stichopus herrmanni, Thelenota ananas,Thelenota anax, Holothuria fuscogilva, Holothuria fuscopunctata, Actinopyga mauritiana, Actinopyga caerulea and Bohadschiaargus) were determined.

RESULTS: All species except T. anax and A. caerulea had higher protein and lower fat levels. A. mauritiana and B. argus had lessash content. Glycine was the dominant amino acid found in all species, and content ranged from 126 to 216 mg g−1 of crudeprotein. All species exhibited low lysine : arginine ratio and higher essential amino acid scores were obtained by threonine andphenylalanine + tyrosine. A. mauritiana had proportionally less saturated fatty acids (31.23%), and more monounsaturatedfatty acids (45.64%) and polyunsaturated fatty acids (PUFA, 23.13%) than other species. Arachidonic acid (C20 : 4n-6) was themajor PUFA in all species. T. ananas, A. mauritiana and A. caerulea contained more n-3 PUFA. The n-3/n-6 ratios of eight seacucumbers species ranged from 0.25 to 0.61.

CONCLUSION: Sea cucumbers are a seafood with high protein and low fat levels. The amino acid contents were similar but fattyacid profiles were different among species. The comparison showed that T. ananas, A. mauritiana and B. argus possessed highernutritional values than other sea cucumber species.c© 2010 Society of Chemical Industry

Keywords: sea cucumber; amino acids; fatty acids; arachidonic acid

INTRODUCTIONSea cucumbers (Echinodermata: Holothuroidea), or their driedform (beche-de-mer), have been a dietary delicacy and medicinalcure for Asians over many centuries.1 The global sea cucumbertrade intended for the food market is controlled by China, HongKong SAR, Singapore and Taiwan Province of China.2 Dependingon the conversion factor used for the dry/wet weight of seacucumbers, it is possible to infer that the combined catches forthe Asia and Pacific regions are of the order of 20 000–40 000 t peryeat.1

As seafood, sea cucumbers are usually processed into a driedproduct known as ‘beche-de-mer’. Beche-de-mer can be rankedas of high, medium or low commercial value based on species,abundance, appearance, odor, color, thickness of the body walland main market demand.3 However, there is no informationabout the evaluation of commercial value on the basis of chemicalcomposition and nutritional quality. Moreover, the ability of thebody wall of Stichopus herrmanni to undergo tissue regenerationafter being cut up and returned to the sea reinforced people’sconfidence concerning the value of the species as traditionalmedicine. In Malaysia, S. herrmanni is widely utilized as a traditionalremedy for asthma, hypertension, rheumatism, sinus, cuts, andburns.4

Currently, the chemical composition of fish and fishery productsis being been widely investigated to analyze their nutritionalquality.5 – 11 Some studies have reported the chemical compositionof sea cucumbers.12,13 However, these are all fresh or frozen

samples. As far as we know, there is no work on determiningthe chemical composition and nutritional quality in sea cucumberproducts.

Therefore, the objectives of this work were to analyze andcompare the proximate composition, amino acid and fatty acidcomposition in dried products of eight common commercial seacucumber species, and to elucidate their nutritional and medicinalvalue to consumers.

MATERIALS AND METHODSSample preparationSamples of dried S. herrmanni, Thelenota ananas, Thelenotaanax, Holothuria fuscogilva, Holothuria fuscopunctata, Actinopygamauritiana, Actinopyga caerulea and Bohadschia argus productswere purchased from a local retail market in Guangzhou, China.There were 30 individuals per sample, with each sample divided

∗ Correspondence to: Chaoqun Hu, South China Sea Institute of Oceanology,Chinese Academy of Sciences, Guangzhou 510301, China.E-mail: [email protected]

a Key Laboratory of Marine Bio-resources Sustainable Utilization (LMB), KeyLaboratory of Applied Marine Biology of Guangdong Province and ChineseAcademy of Sciences (LAMB), South China Sea Institute of Oceanology, ChineseAcademy of Sciences, Guangzhou 510301, China

b Department of Biology, Zhanjiang Normal University, Zhanjiang, 524048, China

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www.soci.org J Wen, C Hu, S Fan

into three groups (10 individuals to each group). The samples wereground using a grinder into a fine powder. The ground portionswere kept in plastic bags pending analysis. From each group 100 gpowder was used in each analysis discussed below.

Proximate chemical compositionMoisture content was determined by drying the sample in anoven at 105 ◦C until a constant weight was obtained. Crudeprotein content was determined by the Kjeldahl method, and aconversion factor of 6.25 was used to convert total nitrogen tocrude protein. Fat was determined by using the Soxhlet extractionmethod. Ash was determined by incineration in a muffle furnaceat 550 ◦C for 24 h.14

Amino acid analysisAmino acid content of samples was measured according to theGB/T14965-1994 in China: the sample was hydrolyzed at 110 ◦C for24 h with 6 mol L−1 HCl; following hydrolysis, 1 mL of hydrolyzatewas with drawn and evaporated to dryness under vacuum at45 ◦C to remove HCl. The hydrolyzate was dissolved in 5 mL of0.02 mol L−1 HCl, and then centrifuged at 5000 rpm and filtered.1 µL of supernatant was used for amino acid analysis, using pre-column OPA and FMOC (for Pro) derivatization. The content oftryptophan was determined by a separate method using alkalinehydrolysis.15 Amino acids were separated by Agilent 1100 HPLC(Palo Alto, CA, USA) using a 4.0 × 125 mm Hypersil ODS C18column. The solvents and gradient conditions were as previouslydescribed.16 Detection wavelengths were set at UV 338 nm and262 nm (for Pro). The identity and quantity of the amino acidswere assessed by comparison with retention times and peakareas of standard amino acids. Essential amino acid scores (EAAS)were also calculated according to FAO/WHO reference amino acidrequirements of adults.17 The amino acid score was calculatedusing the following formula: amino acid score = amount of aminoacid per test protein (mg g−1)/amount of amino acid per proteinin reference pattern (mg g−1) × 100.

Fatty acid analysisFatty acids were extracted and fatty acid methyl esters (FAMEs)were prepared according to the ISO5509 method:18 Soxhletextraction, then saponification, followed by esterification, andfinally extraction of FAMEs in hexane. Gas chromatography(GC) was performed with an Agilent Technologies 6890 gaschromatograph equipped with an HP-5 cross-linked methylsilicone fused-silica capillary column (30 m × 0.32 mm I.D., 0.5 µm

film thickness). Helium was the carrier gas. Oven temperaturewas programmed from 180 to 250 ◦C. Gas chromatography–massspectrometry (GC-MS) was performed on an Agilent Technologies5973 instrument. Individual components were identified usingmass spectral data and by comparing retention time data withthose obtained for authentic and laboratory standards. Peak areawas quantified and expressed as percentage of total fatty acids.

Statistical analysisAll analyses were repeated four times. Results were expressedas mean values ± standard deviation (SD) and one-way analysisof variance (ANOVA) were carried out using a statistical analysissystem (SPSS Version 12). Differences in the concentration ofnutritional elements between species were tested with ANOVAfollowed by multiple-comparison test (Tukey HSD). Differenceswere considered to be significant when P < 0.05.

RESULTS AND DISCUSSIONProximate compositions of the eight sea cucumber speciesProximate compositions are shown in Table 1. Crude proteincontent ranged from 40.7% to 63.3%, crude fat content from 0.3%to 10.1%, and crude ash content from 15.4% to 39.6%. Theseresults were similar to processed Holothuria scabra, which weredetermined to be 39.8–60.2%, 1.2–2.4%, and 17.9–44.5% in theapproximate percentage composition of protein, fat, and ash,respectively.19 Among the three species studied in the presentwork, crude protein content was the highest in A. mauritiana(63.3%) and B. argus (62.1%). All fat contents of sea cucumberspecies were less than 2.0%, except for T. anax (9.9%) andA. caerulea (10.1%). Crude ash content was lowest in A. mauritiana(15.4%) and B. argus (17.7%). The previous studies have reportedthe crude fat content in different fresh or frozen species. Althoughdifferent species were used in their studies, results were found tobe comparable. The crude fat contents were reported to be lowin abyssal sea cucumber species: 2.6% in Oneirophanta mutabilis,3.2% in Peniagone vitrea, 3.8% in Protankyra brychia13 and sometropical species: 1.58% in Euapta godeffroyi, 1.66% in Holothuriapardalis, and 2.42% in Holothuria moebii.12 In the present study,the crude fat contents in S. herrmanni, T. ananas, H. fuscogilva,H. fuscopunctata, A. mauritiana and B. argus were similar to thosementioned above. In particular, the crude fat contents in seacucumbers were lower than the amounts found in many fisheryproducts, for instance in fresh water fish: 5.7% in Channa striatus,9.3% in C. micropeltes, 11.9% in C. lucius;20 in marine fish: 20.1% inPampus punctatissimus;21 and in crabs: 3.6% in Carcinus maenas,22

Table 1. Proximate composition (%) of eight sea cucumbers (mean values ± standard deviation)

Species Moisture Protein Fat Ash

Stichopus herrmanni 10.2 ± 0.32a 47.0 ± 0.36b 0.8 ± 0.02b 37.9 ± 0.33a

Thelenota ananas 15.1 ± 0.29a 55.2 ± 0.38a 1.9 ± 0.01b 25.1 ± 0.30b

Thelenota anax 1.2 ± 0.06c 40.7 ± 0.33c 9.9 ± 0.27a 39.2 ± 0.28a

Holothuria fuscogilva 11.6 ± 0.28a 57.8 ± 0.41a 0.3 ± 0.01c 26.4 ± 0.31b

Holothuria fuscopunctata 7.0 ± 0.14b 50.1 ± 0.38b 0.3 ± 0.01c 39.6 ± 0.24a

Actinopyga mauritiana 11.6 ± 0.31a 63.3 ± 0.43a 1.4 ± 0.02b 15.4 ± 0.18c

Actinopyga caerulea 0.81 ± 0.03c 56.9 ± 0.36a 10.1 ± 0.25a 28.4 ± 0.32b

Bohadschia argus 13.0 ± 0.26a 62.1 ± 0.39a 1.1 ± 0.01b 17.7 ± 0.20c

Values in the same row bearing different letters are significantly different (P < 0.05).

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Table 2. Amino acid profiles (g 100 g−1 wet weight) of eight sea cucumbers (mean values ± standard deviation)

S. herrmanni T. ananas T. anax H. fuscogilva H. fuscopunctata A. mauritiana A. caerulea B. argus

ASP 3.63 ± 0.01b 4.52 ± 0.01a 3.48 ± 0.01b 4.70 ± 0.02a 4.69 ± 0.02a 5.06 ± 0.02a 4.35 ± 0.01a 4.78 ± 0.02a

GLU 5.03 ± 0.01c 5.65 ± 0.01b 4.69 ± 0.03c 7.31 ± 0.02a 6.60 ± 0.02a 6.83 ± 0.03a 6.41 ± 0.02a 6.39 ± 0.02a

SER 1.46 ± 0.02b 2.00 ± 0.02a 1.45 ± 0.02b 2.19 ± 0.01a 1.93 ± 0.01a 2.27 ± 0.02a 2.01 ± 0.01a 2.25 ± 0.01a

HISa 0.29 ± 0.03b 0.38 ± 0.01a 0.25 ± 0.01b 0.27 ± 0.01b 0.31 ± 0.01b 0.40 ± 0.01a 0.32 ± 0.01b 0.49 ± 0.01a

GLY 6.86 ± 0.01b 6.95 ± 0.03b 5.77 ± 0.04c 12.5 ± 0.04a 10.8 ± 0.02a 11.00 ± 0.04a 9.90 ± 0.04a 7.90 ± 0.04b

THRa 1.87 ± 0.02b 2.58 ± 0.01a 1.88 ± 0.01b 2.58 ± 0.01a 2.37 ± 0.01a 2.52 ± 0.01a 2.36 ± 0.02a 2.31 ± 0.01a

ALA 3.27 ± 0.01c 3.59 ± 0.01c 2.95 ± 0.01c 5.74 ± 0.02a 5.27 ± 0.02a 5.77 ± 0.02a 5.24 ± 0.02a 4.39 ± 0.02b

ARG 2.93 ± 0.01c 3.41 ± 0.02b 2.71 ± 0.02c 4.95 ± 0.03a 4.52 ± 0.02a 4.64 ± 0.01a 4.26 ± 0.02a 4.06 ± 0.02a

TYR 0.71 ± 0.02b 1.03 ± 0.01a 0.76 ± 0.02b 0.93 ± 0.01a 0.91 ± 0.01a 1.10 ± 0.01a 0.94 ± 0.01a 1.18 ± 0.01a

VALa 1.34 ± 0.01b 2.12 ± 0.01a 1.65 ± 0.02b 1.81 ± 0.01b 1.72 ± 0.02b 2.18 ± 0.01a 1.80 ± 0.01b 1.97 ± 0.01a

METa 0.44 ± 0.03b 0.21 ± 0.03c 0.42 ± 0.01b 0.57 ± 0.02a 0.44 ± 0.01b 0.62 ± 0.01a 0.65 ± 0.01a 0.62 ± 0.01a

TRPa 0.13 ± 0.02b 0.27 ± 0.01a 0.22 ± 0.03a 0.10 ± 0.01b 0.11 ± 0.01b 0.13 ± 0.01b 0.20 ± 0.01a 0.17 ± 0.01b

PHEa 0.92 ± 0.01b 1.53 ± 0.01a 1.13 ± 0.01b 0.89 ± 0.01b 1.07 ± 0.01b 1.18 ± 0.01b 1.06 ± 0.01b 1.36 ± 0.01a

ILEa 1.08 ± 0.04b 1.57 ± 0.02a 1.16 ± 0.02b 0.94 ± 0.01b 0.88 ± 0.01b 1.47 ± 0.01a 1.31 ± 0.01a 1.51 ± 0.01a

LEUa 1.57 ± 0.02b 2.36 ± 0.01a 1.76 ± 0.01b 1.88 ± 0.02b 1.84 ± 0.02b 2.27 ± 0.02a 2.01 ± 0.01b 2.45 ± 0.01a

LYSa 0.79 ± 0.01b 1.34 ± 0.03a 0.90 ± 0.01b 0.62 ± 0.01b 0.68 ± 0.01b 1.14 ± 0.01a 0.90 ± 0.01b 1.44 ± 0.01a

PRO 2.39 ± 0.02c 2.74 ± 0.01c 2.10 ± 0.02c 5.45 ± 0.03a 5.25 ± 0.03a 5.47 ± 0.03a 4.40 ± 0.03b 4.08 ± 0.03b

TAA 34.73 ± 0.06b 42.27 ± 0.05a 33.32 ± 0.06b 53.40 ± 0.06a 49.41 ± 0.05a 54.13 ± 0.05a 48.10 ± 0.06a 47.27 ± 0.06a

EAA/NEAA 0.49 ± 0.03b 0.60 ± 0.03a 0.57 ± 0.01a 0.38 ± 0.01c 0.39 ± 0.01c 0.44 ± 0.01b 0.45 ± 0.01b 0.53 ± 0.01a

LYS/ARG 0.27 ± 0.01b 0.39 ± 0.01a 0.33 ± 0.01a 0.13 ± 0.01c 0.15 ± 0.01c 0.25 ± 0.01b 0.21 ± 0.01b 0.35 ± 0.01a

Abbreviations: ASP, aspartic acid; GLU, glutamine; SER, serine; HIS, histidine; GLY, glycine; THR, threonine; ALA, alanine; ARG, arginine; TYR, tyrosine;VAL, valine; MET, methionine; TRP, tryptophan; PHE, phenylalanine; ILE, isoleucine; LEU, leucine; LYS, lysine; PRO, proline; TAA, total amino acids;EAA/NEAA, essential amino acids/nonessential amino acids. Values in the same row bearing different letters are significantly different (P < 0.05).a Essential amino acids.

4.25% in Eriocheir sinensis.7 Therefore, these results indicated thatall eight species except T. anax and A. caerulea had higher proteinand lower fat levels.

Amino acid profiles of the eight sea cucumber speciesThe amino acid profiles of the eight sea cucumber species arepresented in Table 2. The most abundant amino acids in all ofthem were glycine, glutamic acid, aspartic acid, alanine, andarginine. These amino acids constituted 58.2–65.9% of the totalamino acids (TAA). Accordingly, the contents of essential aminoacids (EAA) were not high: the ratio of EAA : NEAA ranged from0.38 (H. fuscogilva) to 0.60 (T. ananas). Generally, A. mauritiana hadthe highest amounts of amino acids compared to other species. Ahigh amount of glycine was found in all of species studied in thiswork, the content ranged from 126 to 216 mg g−1 crude protein.

However, these values were found to be significantly higher thanthose reported for fish: 25.9 mg g−1 crude protein in Oreochromisniloticus,23 40.1 mg g−1 crude protein in P. punctatissimus;21 andcrabs: 55.6 mg g−1 crude protein in C. maenas,22 64 mg g−1 crudeprotein in E. sinensis.7 Serum cholesterol profiles may be affectedby the protein and amino acid composition of the diet. Previousstudies have shown that serum total cholesterol level is reducedby glycine.24,25

Several studies have confirmed that low lysine : arginine ratiosignificantly reduced concentrations of cholesterol in the serumand aorta, and suggest that low lysine/arginine ratio of a proteinexerts hypocholesterolemic effects.26,27 In the present study,values of lysine : arginine ranged from 0.13 (H. fuscogilva) to0.39 (T. ananas). Ratios were significant lower than in manyfishery products, including fish: 1.64 in C. striatus,20 1.05 in Clarias

Table 3. Essential amino acid scores of eight sea cucumber

S. herrmanni T. ananas T. anax H. fuscogilva H. fuscopunctata A. mauritiana A. caerulea B. argus

HIS 41b 46b 41b 31c 41b 42b 37b 52a

ILE 76b 95a 95a 54c 59c 77b 77b 81b

LEU 57b 73a 73a 55b 62b 61b 60b 67a

LYS 37b 54a 49a 24c 30c 40b 35b 52a

MET 59b 24c 64b 62b 55b 61b 71a 62b

PHE + TYR 115c 155a 155a 105c 132b 120c 117c 136b

THR 173b 203a 201a 194a 206a 173b 180b 162c

TRP 47b 82a 90a 29c 37c 34c 59b 46b

VAL 90a 98a 104a 80b 88a 88a 81b 81b

Abbreviations are as in Table 2. Values in the same row bearing different letters are significantly different (P < 0.05).

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Table 4. Fatty acid profiles (%) of eight sea cucumbers (mean values ± standard deviation)

S.herrmanni

T.ananas

T.anax

H.fuscogilva

H.fuscopunctata

A.mauritiana

A.caerulea

B.argus

C8 : 0 n.d. n.d. 0.03 ± 0.01a n.d. 0.03 ± 0.01a n.d. n.d. 0.07 ± 0.01a

C10 : 0 n.d. n.d. 0.04 ± 0.01a n.d. 0.08 ± 0.01a n.d. n.d. 0.08 ± 0.01a

C12 : 0 0.12 ± 0.01b 0.07 ± 0.01b 0.33 ± 0.01a 0.06 ± 0.01b 0.06 ± 0.01b 0.07 ± 0.01b 0.02 ± 0.01b 0.90 ± 0.01b

C13 : 0 0.34 ± 0.01a 0.16 ± 0.01b 0.16 ± 0.01b 0.18 ± 0.01b 0.13 ± 0.01b 0.05 ± 0.01b 0.09 ± 0.01b 0.13 ± 0.01b

C14 : 0 2.29 ± 0.09c 7.00 ± 0.12a 7.97 ± 0.21a 5.53 ± 0.21a 4.05 ± 0.16b 1.39 ± 0.02c 4.28 ± 0.15b 3.92 ± 0.12b

C15 : 0 2.46 ± 0.06b 4.86 ± 0.09a 4.27 ± 0.11a 4.56 ± 0.16a 2.84 ± 0.08b 1.17 ± 0.04b 1.89 ± 0.06b 2.54 ± 0.08b

C16 : 0 13.77 ± 0.44c 22.08 ± 0.41b 31.60 ± 0.91a 31.86 ± 0.82a 24.80 ± 0.51b 5.91 ± 0.11d 17.90 ± 0.41c 15.81 ± 0.44c

C17 : 0 3.23 ± 0.04a 3.12 ± 0.02a 2.68 ± 0.06b 2.60 ± 0.06b 2.31 ± 0.04b 1.55 ± 0.02c 1.77 ± 0.03c 2.10 ± 0.03b

C18 : 0 10.26 ± 0.12b 10.09 ± 0.11b 8.93 ± 0.41b 9.29 ± 0.12b 14.13 ± 0.41a 7.14 ± 0.22c 13.68 ± 0.37a 9.98 ± 0.20b

C19 : 0 2.68 ± 0.03a 1.82 ± 0.02b 1.14 ± 0.02c 1.12 ± 0.02c 0.80 ± 0.01c 2.14 ± 0.02b 1.40 ± 0.02c 2.04 ± 0.02b

C20 : 0 4.79 ± 0.16a 2.10 ± 0.04c 1.67 ± 0.04c 1.44 ± 0.03c 2.47 ± 0.03c 5.66 ± 0.14a 4.43 ± 0.12a 3.85 ± 0.08b

C21 : 0 4.07 ± 0.10a 1.98 ± 0.02c 1.33 ± 0.02c 1.33 ± 0.02c 1.98 ± 0.05c 3.49 ± 0.12b 1.77 ± 0.01c 3.22 ± 0.16b

C22 : 0 2.32 ± 0.08a 1.05 ± 0.01b 1.05 ± 0.01b 1.05 ± 0.01b 2.27 ± 0.03a 2.24 ± 0.03a 1.91 ± 0.01a 2.07 ± 0.02a

C23 : 0 0.48 ± 0.01a 0.14 ± 0.01c 0.09 ± 0.01c 0.28 ± 0.01b 0.38 ± 0.01b 0.31 ± 0.01b 0.34 ± 0.01b 0.50 ± 0.01a

C24 : 0 0.37 ± 0.01a 0.24 ± 0.01b 0.29 ± 0.01b 0.20 ± 0.01b 0.22 ± 0.01b 0.11 ± 0.01c 0.06 ± 0.01c 0.19 ± 0.01c∑

SFA 47.20 ± 1.26b 54.70 ± 0.88a 61.60 ± 1.85a 59.50 ± 1.26a 56.55 ± 1.12a 31.23 ± 1.34c 49.54 ± 1.26b 47.40 ± 1.16b

C14 : 1 0.27 ± 0.01a 0.08 ± 0.01b 0.07 ± 0.01b 0.18 ± 0.01a 0.13 ± 0.01b 0.01 ± 0.01b 0.05 ± 0.01b 0.17 ± 0.01a

C16 : 1 n-7 4.50 ± 0.23c 12.46 ± 0.10b 12.77 ± 0.11b 21.03 ± 0.22a 17.59 ± 0.16a 3.42 ± 0.11c 13.48 ± 0.10b 5.48 ± 0.11c

C17 : 1 n.d. 0.18 ± 0.01a 0.04 ± 0.01b 0.04 ± 0.01b n.d. n.d. n.d. n.d.

C18 : 1 n-9 3.78 ± 0.31a 3.16 ± 0.12b 3.15 ± 0.21b 3.77 ± 0.12a 3.33 ± 0.11b 3.27 ± 0.09b 4.22 ± 0.21a 4.30 ± 0.16a

C20 : 1 n-9 16.93 ± 0.32a 6.11 ± 0.09c 5.38 ± 0.12c 4.36 ± 0.12c 9.19 ± 0.22b 20.72 ± 0.42a 10.11 ± 0.10b 13.49 ± 0.30b

C22 : 1 n-9 1.50 ± 0.02b 1.72 ± 0.01b 1.35 ± 0.01b 0.28 ± 0.01c 1.03 ± 0.01b 2.70 ± 0.02a 0.84 ± 0.01b 1.03 ± 0.01b

C23 : 1 n-9 5.27 ± 0.21b 3.52 ± 0.02c 1.67 ± 0.01d 1.17 ± 0.01d 3.47 ± 0.03c 8.49 ± 0.31a 4.29 ± 0.22c 5.74 ± 0.18b

C24 : 1 n-9 5.47 ± 0.18a 2.61 ± 0.06b 2.55 ± 0.08b 1.36 ± 0.01c 3.61 ± 0.10b 7.03 ± 0.11a 3.33 ± 0.06b 6.39 ± 0.12a∑

MUFA 37.70 ± 1.28b 29.80 ± 0.42c 27.00 ± 0.56c 32.19 ± 0.40b 38.35 ± 0.38b 45.64 ± 1.42a 36.32 ± 0.37b 36.60 ± 0.33b

C16 : 2 n-6 0.17 ± 0.01c 0.45 ± 0.01b 0.60 ± 0.01a 0.64 ± 0.01a 0.14 ± 0.01c 0.02 ± 0.01d 0.78 ± 0.01a 0.19 ± 0.01c

C16 : 3 n-3 0.24 ± 0.01a 0.04 ± 0.01b 0.10 ± 0.01b 0.16 ± 0.01b 0.06 ± 0.01b 0.13 ± 0.01b 0.21 ± 0.01a 0.10 ± 0.01b

C18 : 2 n-6 2.02 ± 0.04a 1.08 ± 0.02b 1.21 ± 0.02b 1.23 ± 0.02b 0.87 ± 0.01c 1.16 ± 0.01b 0.70 ± 0.01c 1.40 ± 0.01b

C18 : 3 n-3 1.56 ± 0.03a 0.89 ± 0.01b 0.41 ± 0.01b 0.59 ± 0.01b 0.69 ± 0.01b 1.74 ± 0.02a 0.54 ± 0.01b 0.92 ± 0.02b

C18 : 4 n-3 0.57 ± 0.01b 0.88 ± 0.01a 0.33 ± 0.01b 0.33 ± 0.01b 0.18 ± 0.01c 0.40 ± 0.01b 0.54 ± 0.01b 0.27 ± 0.01b

C20 : 2 n-6 1.32 ± 0.02a 0.64 ± 0.01b 0.65 ± 0.01b 0.37 ± 0.01c 1.02 ± 0.02a 1.42 ± 0.01a 1.31 ± 0.01a 1.24 ± 0.01a

C20 : 4 n-6 (AA) 7.90 ± 0.36b 7.54 ± 0.21b 5.03 ± 0.22c 3.76 ± 0.04c 1.82 ± 0.02d 14.42 ± 0.41a 6.53 ± 0.21b 9.92 ± 0.33b

C20 : 5 n-3 (EPA) 1.31 ± 0.09b 3.92 ± 0.04a 3.10 ± 0.09a 1.24 ± 0.01b 0.32 ± 0.01c 3.84 ± 0.09a 3.53 ± 0.10a 1.96 ± 0.04b∑

PUFA 15.10 ± 0.57b 15.40 ± 0.32b 11.40 ± 0.38b 8.32 ± 0.28c 5.10 ± 0.16d 23.13 ± 0.48a 14.14 ± 0.37b 16.00 ± 0.38b∑

n-6 11.20 ± 0.43b 9.26 ± 0.25b 6.89 ± 0.26c 6.00 ± 0.24c 3.85 ± 0.15d 17.02 ± 0.36a 9.32 ± 0.28b 12.75 ± 0.44b∑

n-3 3.44 ± 0.14b 5.69 ± 0.07a 3.84 ± 0.12b 2.32 ± 0.11c 1.25 ± 0.06d 6.11 ± 0.08a 4.82 ± 0.11a 3.25 ± 0.13b

n-6/n-3 3.26 ± 0.14b 1.63 ± 0.09c 1.79 ± 0.07c 2.59 ± 0.11b 3.08 ± 0.11b 2.79 ± 0.06b 1.93 ± 0.08c 3.92 ± 0.13a

n-3/n-6 0.31 ± 0.14b 0.61 ± 0.09a 0.56 ± 0.07a 0.39 ± 0.11b 0.32 ± 0.06b 0.36 ± 0.06b 0.52 ± 0.08a 0.25 ± 0.13b

Abbreviations: SFA, saturated fatty acids; MUFA, monounsaturated fatty acids; PUFA, polyunsaturated fatty acids; n.d., not detected. Values in thesame row bearing different letters are significantly different (P < 0.05), whereas values without letters indicate no significant differences.

anguillaris,23 1.49 in P. punctatissimus;21 crabs: 0.88 in C. maenas,22

0.82 in E. sinensis;7 and shrimps: 0.96 in Penaeus semisulcatus, 0.85in Metapenaeus monoceros.6 In Malaysia, S. herrmanni was widelyutilized as a traditional remedy for hypertension.4 Therefore, theseresults indicated that all species studied in this work were an idealfood for people with hyperlipidemia.

The essential amino acids scores are presented in Table 3.Generally, threonine and phenylalanine + tyrosine had the highestscores in all species. Lysine, methionine, and histidine were foundto be the first limiting amino acids in all species. Although histidinewould have been described as the limiting amino acid in them,the essential amino acids most often acting in a limiting capacityare lysine, methionine, threonine, and tryptophan.28 Therefore,lysine would be the real limiting amino acid. However, in Chineserecipes, sea cucumber is often cooked with pork, mutton and

tremella (yiner, the silvery tree mushroom), which will supply thelimiting amino acid.29

Fatty acid profiles of the eight sea cucumber speciesThe profiles and levels of fatty acids are given in Table 4. The fattyacid profiles were different between species. The profiles of allspecies were dominated by saturated fatty acids (SFA), except A.mauritiana (31.23% of total fatty acids) and palmitic acid (C16 : 0,13.77–31.86% of total fatty acids) was the major SFA in all speciesexcept A. mauritiana (stearic acid, C18 : 0, 7.14% of total fatty acids).A. mauritiana had proportionally less SFA, particularly palmitic acid(C16 : 0) and stearic acid (C18 : 0), than other species, but highermonounsaturated fatty acids (MUFA, 45.64% of total fatty acids),especially eicosenoic acid (C20 : 1n-9, 20.72% of total fatty acids),which was the dominant fatty acid. Palmitoleic acid (C16 : 1n-7)


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Chemical composition and nutritional quality of sea cucumbers www.soci.org

Table 5. Nutritional composition statistical differences between species, with respective P-values (P < 0.05)

Species

Protein (T. ananas = A. mauritiana = B. argus = H. fuscogilva = A. caerulea) > (S. herrmanni = H. fuscopunctata) > T. anax

Fat (H. fuscogilva = H. fuscopunctata) < (T. ananas = A. mauritiana = B. argus = S. herrmanni) < (A. caerulea = T. anax)

Ash (A. mauritiana = B. argus) < (T. ananas = H. fuscogilva = A. caerulea) < (S. herrmanni = H. fuscopunctata = T. anax)

HIS B. argus > (T. ananas = A. mauritiana = S. herrmanni = A. caerulea = H. fuscopunctata = T. anax) > H. fuscogilva

ILE (T. ananas = T. anax) > (A. mauritiana = B. argus = S. herrmanni = A. caerulea) > (H. fuscogilva = H. fuscopunctata)

LEU (T. ananas = B. argus = T. anax) > (A. mauritiana = S. herrmanni = A. caerulea = H. fuscogilva = H. fuscopunctata)

LYS (T. ananas = B. argus = T. anax) > (A. mauritiana = S. herrmanni = A. caerulea) > (H. fuscogilva = H. fuscopunctata)

MET A. caerulea > (A. mauritiana = B. argus = S. herrmanni = A. caerulea = H. fuscogilva = H. fuscopunctata) > T. ananas

PHE + TYR (T. ananas = T. anax) > (B. argus = H. fuscopunctata) > (A. mauritiana = S. herrmanni = A. caerulea = H. fuscogilva)

THR (T. ananas = T. anax = H. fuscogilva = H. fuscopunctata) > (A. mauritiana = S. herrmanni = A. caerulea) > B. argus

TRP (T. ananas = T. anax) > (B. argus = S. herrmanni = A. caerulea) > (A. mauritiana = H. fuscogilva = H. fuscopunctata)

VAL (T. ananas = A. mauritiana = S. herrmanni = T. anax = H. fuscopunctata) > (B. argus = A. caerulea = H. fuscogilva)

EAA/NEAA (T. ananas = B. argus = T. anax) > (A. mauritiana = S. herrmanni = A. caerulea) > (H. fuscogilva = H. fuscopunctata)∑

SFA A. mauritiana < (B. argus = S. herrmanni = A. caerulea) < (T. ananas = T. anax = H. fuscogilva = H. fuscopunctata)∑

MUFA A. mauritiana > (B. argus = S. herrmanni = A. caerulea = H. fuscogilva = H. fuscopunctata) > (T. ananas = T. anax)∑

PUFA A. mauritiana > (T. ananas = B. argus = S. herrmanni = A. caerulea = T. anax = H. fuscopunctata) > H. fuscogilva

C20 : 4 n-6 (AA) A. mauritiana > (T. ananas = B. argus = S. herrmanni = A. caerulea) > (T. anax = H. fuscogilva) >H. fuscopunctata

C20 : 5 n-3 (EPA) (T. ananas = A. mauritiana = A. caerulea = T. anax) > (B. argus = S. herrmanni = A. caerulea) > H. fuscopunctata∑

n-3 PUFA (T. ananas = A. mauritiana = A. caerulea) > (B. argus = S. herrmanni = T. anax) > H. fuscogilva > H. fuscopunctata

Abbreviations are as in Tables 2 and 4.

was the major MUFA in T. ananas (12.46%), T. anax (12.77%),H. fuscogilva (21.03%), H. fuscopunctata (17.59%) and A. caerulea(13.48%), but was less in S. herrmanni (4.50%), A. mauritiana(3.42%) and B. argus (5.48%). Moreover, A. mauritiana containedhigher polyunsaturated fatty acids (PUFA, 23.13% of total fattyacids) and n-3 PUFA (6.11% of total fatty acids) than other species.Compared with those reported for abyssal, tropical, and temperatesea cucumbers,12,13 the species studied in this work had higheramounts of SFA and MUFA, but lower amounts of PUFA. Thisdiscrepancy may be attributable to numerous factors, diet andambient temperature being particularly important.30 Moreover,the differences were reasonable due to the processing treatmentof dried sea cucumber product. Once caught, sea cucumberis gutted, boiled and dried.31 A previous study confirmed thatprocesses, especially heating, have a considerable effect on fattyacid compositions in food.9

The principal n-6 PUFA was arachidonic acid (AA, 20 : 4 n-6)in all species. Similar contents were reported for abyssal seacucumber species,13 whereas higher values were reportedfor tropical species.12 Moreover, high contents of AA werereported for fish6,11,20 and green crab.8 AA is the main precursorof eicosanoids,32 the major component of cell membranephospholipids, and is the predominant long-chain PUFA of thecentral nervous system.33 Apart from this function, AA also plays arole in growth. Moreover, AA is known to be responsible for bloodclotting in wound healing, it will interfere with the blood clottingprocess and attach to endothelial cells during wound healing.34

This is a good explanation for why S. herrmanni was widely utilizedas a traditional remedy for cuts and burns in Asia.4

Eicosapentaenoic acid (EPA, C20 : 5n-3) was the primary n-3PUFA in T. ananas (3.92%), T. anax (3.10%), A. mauritiana (3.84%),A. caerulea (3.53%), and B. argus (1.96%), but was less inS. herrmanni (1.31%), H. fuscogilva (1.24%), and H. fuscopunctata(0.32%). Unfortunately, docosahexaenoic acid (DHA, C22 : 6 n-3)was not detected in all species. EPA and DHA are associated

with decreased risk of coronary heart disease and cancer.35,36 Inprevious studies, EPA and DHA were the major n-3 PUFA in freshand frozen sea cucumbers.12,13 The loss of DHA was reasonabledue to the processing treatment of dried sea cucumber products,such as repeated boiling.29 The long-chain PUFAs in fish and fishoils, such as EPA and DHA, are considered to be highly susceptibleto oxidation during heating and other culinary treatments.37

The n-3/n-6 ratios of eight sea cucumbers species ranged from0.25 to 0.61. These values were similar to those reported fortropical species (0.41–0.89),13 and lower than those reportedfor abyssal species (1.74–2.75).12 The results indicated that, justlike fish, differences in fatty acids of sea cucumbers are basedon their environmental conditions, especially water temperature,which can influence fatty acid composition.38 FAO experts haverecommended that the ratio of n-3:n-6 in the diet should bebetween 1 : 8 and 2:5.39 Therefore, these results indicated that allsea cucumber species in the diet may contribute to maintain therecommended n-3:n-6 ratio.

Comparative nutritional quality of the eight sea cucumberspeciesAll the relative nutritional values mentioned above were com-pared, where high values correspond to better-quality foods.Table 5 shows that T. ananas, A. mauritiana, B. argus, H. fuscogilva,and A. caerulea contained more protein; A. mauritiana and B. argushad less ash content; T. ananas, B. argus, and T. anax containedmore essential amino acids; A. mauritiana had less SFA, and moreMUFA and PUFA; and T. ananas, A. mauritiana, and A. caeruleacontained more n-3 PUFA. In this case, the higher values wereobtained in T. ananas, A. mauritiana and B. argus.

ACKNOWLEDGEMENTSThis work was supported by the National Key Technologies R&DProgram (2009BAB44B02), the Science and Technology Program

J Sci Food Agric 2010; 90: 2469–2474 c© 2010 Society of Chemical Industry wileyonlinelibrary.com/jsfa

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of Guangdong Province (2009B091300155, 2007A020300007-15,A200899E02, A200901E01), and Guangxi Province (0815006-2).

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