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Food Additives & Contaminants: Part B: Surveillance Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tfab20
Elemental composition of commercial sea cucumbers (holothurians) J. Wen
a b
& C. Hu
a
a
Key Laboratory of Marine Bio-resources Sustainable Utilization (LMB), Key Laboratory of Applied Marine Biology of Guangdong Province and The Chinese Academy of Sciences (LAMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China b
Department of Biology, Zhanjiang Normal University, Zhanjiang 524048, China Published online: 25 Nov 2010.
To cite this article: J. Wen & C. Hu (2010) Elemental composition of commercial sea cucumbers (holothurians), Food Additives & Contaminants: Part B: Surveillance, 3:4, 246-252, DOI: 10.1080/19393210.2010.520340 To link to this article: http://dx.doi.org/10.1080/19393210.2010.520340
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Food Additives and Contaminants: Part B Vol. 3, No. 4, December 2010, 246–252
VIEW DATASET Elemental composition of commercial sea cucumbers (holothurians) J. Wenab and C. Hua* a
Key Laboratory of Marine Bio-resources Sustainable Utilization (LMB), Key Laboratory of Applied Marine Biology of Guangdong Province and The Chinese Academy of Sciences (LAMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China; bDepartment of Biology, Zhanjiang Normal University, Zhanjiang 524048, China
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(Received 24 July 2010; final version received 30 August 2010) Toxic and essential elements in 11 different sea cucumber species were determined and compared with daily intake recommendations and maximum allowed levels. The contents of macro-elements contents in dried sea cucumber samples were found to be 25,000–152,000 mg kg–1 for Na, 4000–8600 mg kg1 for Mg, 1100–5200 mg kg1 for K, 15,000–68,000 mg kg1 and 36,300–251,000 mg kg1 for Cl. Trace element concentrations in dried sea cucumber samples were found to be 11–100 mg kg1 for Zn, 41–660 mg kg1 for Fe, 3–74 mg kg1 for Cu, 1.1–16 mg kg1 for Mn, 1.4–3.7 mg kg1 for Se, 1.1–9.6 mg kg1 for Cr, and 0.3–5.1 mg kg1 for Ni. All sea cucumber species were rich sources of Na, Cl, Mg, Ca, Fe, Cu, Se and Cr for human consumption. Regarding contaminants, As, Cd and Pb concentrations in dried sea cucumbers were in the ranges of 1.1–6.1, 0.03–0.06 and 0.11–0.69 mg kg1, respectively. Moreover, Hg values of 11 sea cucumbers were below the detection limit (0.01 mg kg1). Keywords: animal products; meat; metals
Introduction Sea cucumbers (also called holothurians) are an enigmatic and diverse group of echinoderms. They are slowmoving invertebrates that can live on sand, mud, rock and reef flats, often related with seaweeds, coral and sea grasses. Most sea cucumbers are detritivores, which is a key role within the marine ecosystem, as they conduct functions including nutrient recycling (Uthicke 2001) and bioturbation (Uthicke 1999). As a kind of seafood, sea cucumbers have a high nutritional value due to their high-protein, low-fat content, amino acid and fatty acid profiles, and they have been regarded as a traditional delicacy, medicine and aphrodisiac in Asia over many centuries. The main use for sea cucumbers as food is for the consumption of the body wall, mostly as a dried product known as ‘beche-de-mer’. Once caught, sea cucumbers are gutted, boiled, and salted and dried (Bruckner 2005). Depending on the conversion factor used for the dry/ wet weight of sea cucumbers, it is possible to infer that the combined catches for the Asia and Pacific regions are in the order of 20,000–40,000 tonnes year1. Sea cucumber species are commercially exploited as food with most of them comprising tropical and sub-tropical species from the families Holothuriidae and
*Corresponding author. Email: [email protected] ISSN 1939–3210 print/ISSN 1939–3229 online ß 2010 Taylor & Francis DOI: 10.1080/19393210.2010.520340 http://www.informaworld.com
Stichopodidae, including the genuses Holothuria, Actinopyga, Bohadschia and Stichopus (Food and Agricultural Organization (FAO) 2008). Essential elements (e.g. Na, Mg, Cl, K, Ca, Mn, Fe, Cu, Zn, Se and Cr) play important roles in biological systems. On the other hand, environmental contaminants (e.g. As, Cd, Hg and Pb) are a major concern in aquatic environments because they are toxic, even in trace amounts. In recent years, attention has been focused on the determination of elements in seafood due to the nutritional benefits of essential elements and toxicological concerns related to contaminants. In the last decade, the essential and toxic elements of fish, clams and crustaceans have been investigated worldwide (Yilmaz and Yilmaz 2007; Barrento et al. 2008; Turkmen et al. 2008, 2009; Mohapatra et al. 2009; Ozden et al. 2009; Tuzen 2009; Mendil et al. 2010; Ersoy and Celik 2010). However, information on the essential and toxic elements of sea cucumber species in food products is lacking. In this context, the aim of this paper was to quantify the essential elements and contaminants contents in the dried products of 11 sea cucumber species, and to compare such values with the daily intake recommendations and maximum limit levels.
Food Additives and Contaminants: Part B Materials and methods
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Sampling Samples of dried Stichopus herrmanni (curryfish), Stichopus chloronotus (greenfish), Thelenota ananas (prickly redfish), Thelenota anax (amberfish), Holothuria scabra (sandfish), Holothuria mexicana (donkey dungfish), Holothuria fuscogilva (white teatfish), Holothuria fuscopunctata (elephant trunkfish), Actinopyga mauritiana (surf redfish), Actinopyga caerulea (blackfish) and Bohadschia argus (tigerfish) products were purchased from a local retail market and supermarket in Guangzhou, China. There were 30 individuals per sample, each sample divided into three groups (ten individuals per group). The samples were ground using a grinder into a fine powder. The ground portions were kept in a plastic bag pending analysis. From each group 100 g powder were used in each analysis discussed below.
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the concentration of elements per 100 g serving portion was calculated and compared with the recommended intake and limits set by international authorities. The average intakes of the essential elements Na, Cl, K, Ca, Mn and Cr were compared with the daily adequate intakes (AI); Mg, Fe, Cu, Zn and Se were compared with the daily dietary reference intake (DRI); and Na, Cl, Ca, Mn, Fe, Cu, Zn and Se were compared with the daily tolerable upper intake levels (UL). AI, DRI and UL were set by the US Department of Agriculture (USDA) for adult females and males aged between 19 and 50 years. The contaminants Cd and Hg were compared with the maximum allowed level (ML) set by the European Commission; As was evaluated in terms of the action level (AL; similar in meaning to the ML) set by the US Food and Drug Administration (USFDA).
Statistical analysis Elemental analyses Element analyses were performed in the China National Analytical Center, Guangzhou. The element content of samples was pre-treated according to the GB/T 5009.12-2003 in China. Each sample was placed in a Teflon digestion vessel with 7 ml of concentrated (65%) nitric acid (HNO3) and 1 ml of 30% hydrogen peroxide (H2O2). The sample in the vessel containing concentrated nitric acid was then subjected to a microwave programme as follows: 25–200 C for 10 min at 1000 W and 200 C for 10 min at 1000 W. Digests were finally made up with deionised water to 25 ml in acid-washed standard flasks. A blank digest was carried out in the same way. Na, Mg, K, Ca, Zn, Cu and Fe were determined by inductively coupled plasma atomic emission spectrometry (ICP-AES) (SPECTRO CIROSCCD) according to the JY/T 0151996 in China. Mn, Se, Cr, Ni, As, Pb and Cd were also measured by inductively coupled plasma mass spectrometry (ICP-MS) (Agilent 7500a) according to the Pharmacopoeia of the People’s Republic of China (2005 edn), Pt 1, Appx XI D in China. Hg was measured by a Zeeman mercury spectrometer (RA915þ) according to the GB/T 15337-2008 in China. Cl was measured by an automatic potentiometric titrator (Metrohm 751 GPD Tirino) according to the GB/T 9695.8-2008 in China. The element standard solutions used for calibration were prepared by diluting stock solutions of 1000 mg l1 of each element supplied from Sigma (St Louis, MO, USA). Element concentrations were calculated on a mg kg1 dry weight basis.
Nutritional quality and potential risks for consumers To evaluate the elemental nutritional quality and potential consumption hazards of sea cucumbers,
All analyses were repeated four times. Results are expressed as means standard deviation (SD), and one-way analysis of variance (ANOVA) was carried out using a statistical analysis system (SPSS Version 12). Differences in the concentration of nutritional elements between species were tested with ANOVA followed by a multiple-comparison test (Tukey HSD). Differences were considered to be significant at p 5 0.05.
Results and discussion The average macro-elements of each sea cucumber are shown in Table 1. Eleven sea cucumbers were excellent sources of macro-elements (Na, Cl, Ca and Mg). The dried sea cucumber products had significantly higher concentrations of Na and Cl. There is no doubt that these elements come from salt (NaCl) during the processing of drying the sea cucumbers. Among the 11 sea cucumbers, H. scabra, A. mauritiana and B. argus had significantly lower Na and Cl concentrations than other species. These differences might reflect distinct salt requirements for the processing of each species. Although the concentrations of Na and Cl from all dried sea cucumbers were above the daily tolerable upper intake levels (UL), dried sea cucumbers were rehydrated by soaking, which is required for preparation for cooking (Zhong et al. 2007). Thus, the excess Na and Cl will decrease during the rehydration processing. The Ca concentrations of sea cucumbers were significant higher than edible tissue from other fishery products, including fish (Orban et al. 2007; Ersoy and Celik 2010), crabs (Chen et al. 2007; Barrento et al. 2009a), shrimps (Yanar and Clelik 2006) and lobsters (Barrento et al. 2008). Sea cucumbers have a reduced skeleton of isolated, microscopic
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Table 1. Mean macro-elemental composition (SD) (mg kg–1 dry weight) in sea cucumbers.a
S. hermanni S. chloronotus T. ananas T. anax H. fuscogilva H. fuscopunctata H. scabra H. mexicana A. mauritiana A. caerulea B. argus
Na AI ¼ 15000 UL ¼ 23000
Mg DRI ¼ 4200 UL ¼ NS
K AI ¼ 47000 UL ¼ NS
Ca AI ¼ 10000 UL ¼ 25000
Cl AI ¼ 23000 UL ¼ 36000
112000 28000a 152000 36000a 105000 27000a 140000 32000a 83000 14000b 107000 26000a 35000 6000c 65000 9000b 28000 5000c 153000 36000a 25000 4000c
6200 600b 6400 300b 5700 200b 6600 300b 8000 300a 7800 600a 6200 300b 4000 200c 7000 600b 8600 400a 8300 400a
1800 200b 1900 200b 1300 100c 2200 100b 1100 100c 1100 100c 2400 200b 1800 200b 2700 200b 5200 200a 2000 100b
25000 4000b 26000 4000b 15000 2000c 19000 2000b 20000 3000b 50000 6000a 67000 6000a 68000 6000a 16000 2000c 23000 4000b 40000 3000a
175000 38000b 196000 39000b 172000 29000b 251000 45000a 154000 23000b 173000 27000b 51600 4900c 114000 12000b 43600 4500c 202000 36000b 36300 2700c
Notes: aValues in the same row bearing different letters are significantly different ( p 5 0.05). DRI, daily dietary reference intake; AI, daily adequate intakes; UL, daily tolerable upper intake levels; and NS, have not been set.
ossicles embedded in a pliable body wall (Kerr and Kim 2005). It was reasonable that the dermal finer ossicles of sea cucumbers were the source of Ca, because the main composition of ossicles was CaCO3. Ca is nutritionally very important as it provides rigidity to the skeleton and plays a role in many metabolic processes (Food and Agricultural Organization/World Health Organization (FAO/ WHO) 2002). Although the Ca concentrations of S. chloronotus, H. fuscopunctata, H. scabra, H. mexicana and B. argus were above the UL, urinary Ca rises very slowly with intake (slope of 5–10%) and the risk of kidney stones from dietary hypercalciuria must therefore be negligible (FAO/WHO 2002). The concentrations of K varied from 1100 to 5200 mg kg1. These results were similar to those reported for fishes (Ersoy and Celik 2010), crabs (Barrento et al. 2009a), shrimps (Yanar and Clelik 2006) and lobsters (Barrento et al. 2008). Concentrations of seven trace elements were studied from the 11 sea cucumbers (Table 2). Mean Zn concentrations of sea cucumbers ranged from 11 (H. fuscogilva) to 100 mg kg1 (B. argus). This result was similar to those reported for fish: 35.4–106 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 38.8–93.4 mg kg1 in fish species from the Black Sea (Tuzen 2009), 66 mg kg1 in Alosa immaculate (Visnjic-Jeftic et al. 2010), 17.8 mg kg1 in Mulus barbatus ponticus and 25.7 mg kg1 in Trachurus trachurus (Mendil et al. 2010), 11.6–63.5 mg kg1 in fish species from the river (Mendil et al. 2010), 8.1–98.5 mg kg1 in fish species from the Eastern Mediterranean (Ersoy and Celik 2010); for crabs: 47–69.9 mg kg1 in Callinectes sapidus, 37.2–46.8 mg kg1 in Portunus pelagicus (Gokodlu and Yerlikaya 2003), 33–91 mg kg1 in Eriocheir sinensis (Chen et al. 2007), 16–90 mg kg1 in Cancer
pagurus (Barrento et al. 2009a); and for lobsters: 26 mg kg1 in Homarus gammarus and 29 mg kg1 in Homarus americanus (Barrento et al. 2008). The Zn contents of sea cucumbers were higher than those reported in the fish Pagrus pagrus (0.61 mg kg1; Miniadis-Meimaroglou et al. 2007) and fish Perca fluviatilis (5.8–7.4 mg kg1; Orban et al. 2007). The Zn values in the present study were lower than those reported as 288–322 mg kg1 in the crab Scylla serrata (Mohapatra et al. 2009). Zn plays an essential role in a number of biological processes involved in growth and development. It is an essential component of several enzymes participating in the synthesis and degradation of carbohydrates, lipids, proteins and nucleic acids. Additionally, this element has also an essential role in the process of gene expression, particularly in polynucleotide transcription (FAO/WHO 2002). Fish, fruit and greenleaf vegetables are considered to be poor sources of Zn (510 mg kg1), whilst lean meat, cereals and legumes are rich Zn sources (25–50 compared with 11–100 mg kg1 in 11 sea cucumbers) (FAO/ WHO 2002). Zn levels in analysed sea cucumbers were found to be lower than the UL (40 mg day1). The result indicated that the consumption of 100 g of the examined sea cucumbers covers a satisfactory percentage of the human diet. The average Fe concentrations of sea cucumbers were different among species. The lowest and highest Fe levels in sea cucumber species were found to be 41 mg kg1 in A. caerulea and 660 mg kg1 in A. mauritiana. The previous studies showed that the Fe concentrations of fish were varied among species: 68.6–163 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 36.2–145 mg kg1 in fish species from the Black Sea (Tuzen 2009), 9.2–136 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009),
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Table 2. Mean trace elemental composition (SD) (mg kg–1 dry weight) in the sea cucumbers.a
S. hermanni S. chloronotus T. ananas T. anax H. fuscogilva H. fuscopunctata H. scabra H. mexicana A. mauritiana A. caerulea B. argus
Zn DRI ¼ 110 UL ¼ 400
Fe DRI ¼ 180 UL ¼ NS
Cu DRI ¼ 9 UL ¼ 100
Mn AI ¼ 23 UL ¼ 110
Se DRI ¼ 0.55 UL ¼ 4
Cr AI ¼ 0.35 UL ¼ NS
Ni DRI ¼ NS UL ¼ 10
33 3.0c 16 2.0d 46 5.0b 28 2.0c 11 2.0d 25 2.0c 77 6.0a 16 2.0d 57 3.0b 20 1.0c 100 19a
94 27c 80 23c 210 39b 200 30b 250 36b 100 20c 130 19c 190 29b 660 36a 41 6.0d 330 41b
3.0 1.0d 3.0 1.0d 44 3.0b 4.0 1.0d 57 5.0b 74 9.0a 18 3.0c 30 2.0b 14 2.0c 4.0 1.0d 18 3.0c
9.1 0.4b 2.2 0.2d 16 1.6a 10 0.9b 9.4 0.3b 12 0.6b 1.4 0.1d 1.6 0.2d 9.2 0.5b 1.1 0.1d 3.7 0.1c
1.7 0.2b 1.4 0.2b 3.7 1.0a 2.5 0.3b 2.6 0.3b 2.1 0.2b 2.4 0.2b 3.5 0.6a 0.9 0.1c 3.2 0.9a 2.4 0.2b
1.6 0.2c 1.5 0.1c 2.7 0.3c 1.5 0.1c 1.3 0.1c 5.5 0.5b 1.1 0.1c 2.2 0.2c 9.6 0.9a 1.3 0.1c 4.9 0.6b
0.3 0.1c 0.3 0.1c 2.5 0.6a 0.7 0.2c 1.5 0.5b 3.0 0.7a 0.6 0.2c 1.1 0.3b 4.2 0.9a 0.5 0.1c 5.1 1.0a
Notes: aValues in the same row bearing different letters are significantly different ( p 5 0.05). DRI, daily dietary reference intake; AI, daily adequate intakes; UL, daily tolerable upper intake levels; and NS, have not been set.
9.6–107.2 mg kg1 in fish species from the Black Sea (Mendil et al. 2010), 6.5–116 mg kg1 in fish species from the river (Mendil et al. 2010), and 26.8– 453 mg kg1 in fish species from the Eastern Mediterranean (Ersoy and Celik 2010). In general, the concentration levels of Fe in sea cucumbers were higher than those reported in crabs (4.5–6.8 mg kg1 in P. pelagicus, 10.4–11.3 mg kg1 in C. sapidus; Gokodlu and Yerlikaya 2003; and 2.2–4.3 mg kg1 in C. pagurus; Barrento et al. 2009a), shrimps (13.6–16.3 mg kg1; Yanar and Clelik 2006) and lobster (18–23 mg kg1; Barrento et al. 2008). Fe has several vital functions in humans, such as carrying oxygen to tissues by red blood cell haemoglobin, as a transport medium for electrons within cells, and as part of important enzyme systems in various tissues (FAO/WHO 2002). Among 11 sea cucumber species, the Fe concentrations of T. ananas, T. anax, H. fuscogilva, H. mexicana, A. mauritiana and B. argus were above the DRI (18 mg day1). Therefore, the six sea cucumber species are excellent source of Fe. The mean Cu concentrations of sea cucumbers ranged from 3 (S. hermanni and S. chloronotus) to 74 mg kg1 (H. fuscopunctata). Among the 11 sea cucumber species, the Cu contents of S. hermanni, S. chloronotus, T. anax, H. scabra, A. mauritiana, A. caerulea and B. argus (ranging from 3 to 18 mg kg1) were similar to those reported for the muscle of crabs: 14.9–20.8 mg kg1 in P. pelagicus (Gokodlu and Yerlikaya 2003), 16 mg kg1 in E. sinensis (Chen et al. 2007), 6.7–10 mg kg1 in C. pagurus (Barrento et al. 2009a); and muscle of lobsters: 9.6 mg kg1 in H. gammarus and 10 mg kg1 in H. americanus (Barrento et al. 2008). However, the Cu values of sea cucumbers were higher than fish: 0.7– 1.8 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 0.7–2.8 mg kg1 in fish
species from the Black Sea (Tuzen 2009), 0.5– 7.1 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009), 1.4– 1.9 mg kg1 in fish species from the Black Sea (Mendil et al. 2010), and 1.0–2.5 mg kg1 in fish species from the river (Mendil et al. 2010). Cu is found in several enzymes, including the cytochrome c oxidase and the superoxide dismutase, and is used for biological electron transport (Walker et al. 2001). The concentrations of T. ananas, H. fuscogilva, H. fuscopunctata, H. scabra, H. mexicana, A. mauritiana and B. argus were reached the DRI and are below the UL. Therefore, the seven sea cucumber species are excellent source of Cu. Mn is one of vital important essential trace element. It is not only a structural component of some enzymes, but also triggers the actions of some enzymes. The concentrations of Mn in sea cucumber species ranged from 1.1 (A. caerulea) to 16 mg kg1 (T. ananas). The Mn values of sea cucumbers were similar to those reported for fish: 1.3–7.4 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 2.8– 9.1 mg kg1 in fish species from the Black Sea (Tuzen 2009a), 0.4–8.7 mg kg1 in fish species from the Black Sea (Mendil et al. 2010), and 1.0–9.4 mg kg1 in fish species from the river (Mendil et al. 2010). Moreover, the Mn contents of sea cucumbers were higher than crabs: 0.6–1.6 mg kg1 in P. pelagicus (Gokodlu and Yerlikaya 2003), 0.9 mg kg1 in E. sinensis (Chen et al. 2007), 0.2–0.3 mg kg1 in C. pagurus (Barrento et al. 2009a); and lobsters: 0.4 mg kg1 in H. gammarus and 0.6 mg kg1 in H. americanus (Barrento et al. 2008). Among the 11 sea cucumber species, T. ananas and H. fuscopunctata are good sources of Mn. The Se concentrations of sea cucumbers ranged from 1.4 (S. chloronotus) to 3.7 mg kg1 (T. ananas). These values were higher than those reported for fish
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Table 3. Mean contaminant composition (standard deviation) (mg kg1 dry weight) in the sea cucumbersa.
S. hermanni S. chloronotus T. ananas T. anax H. fuscogilva H. fuscopunctata H. scabra H. mexicana A. mauritiana A. caerulea B. argus
As AL ¼ 76
Cd ML ¼ 0.5
Hg ML ¼ 0.5
Pb ML ¼ NS
2.5 0.1b 1.7 0.1b 5.1 0.2a 2.8 0.1b 1.1 0.1c 2.0 0.1b 3.8 0.1b 6.1 0.2a 2.1 0.1b 3.3 0.1b 3.2 0.1b
0.03 0.01a 0.06 0.01a 0.03 0.01a 0.04 0.01a 0.04 0.01a 0.04 0.01a 0.03 0.01a 0.03 0.01a 0.05 0.01a 0.06 0.01a 0.03 0.01a
BDL BDL BDL BDL BDL BDL BDL BDL BDL BDL BDL
0.52 0.03a 0.12 0.01c 0.55 0.03a 0.25 0.02b 0.56 0.03a 0.69 0.06a 0.13 0.01c 0.56 0.03a 0.11 0.01c 0.15 0.01c 0.13 0.01c
Notes: aValues in the same row bearing different letters are significantly different ( p 5 0.05). AL, action level; ML, maximum allowed level; BDL, blow detection limit; and NS, have not been set.
(0.2–0.9 mg kg1 in fish species from the Black Sea; Tuzen 2009a), crab (0.7–1.1 mg kg1 in C. pagurus; Barrento et al. 2009a) and lobsters (0.6 mg kg1 in H. gammarus and 0.9 mg kg1 in H. americanus; Barrento et al. 2008). Se is recognised as an essential micronutrient in animal and humans. The previous study has reported the Se-protective action, especially selenite, on many toxicological effects of Cd and Hg (Early et al. 1992). Se is also implicated in the protection of body tissues against oxidative stress, the maintenance of defences against infection, and modulation of growth and development (FAO/WHO 2002). Worldwide, Se availability in sediments and live organisms shows great variability due to distinct environmental conditions and agricultural practices (FAO/WHO 2002). Thus, as a benthonic organism, sea cucumbers are rich in Se. In the present study, the concentrations of Se in all 11 sea cucumbers were significantly higher than the DRI and are below the UL. Sea cucumbers are therefore an excellent source of Se. Cr levels in analysed sea cucumbers ranged from 1.1 (H. scabra) to 9.6 mg kg1 (A. mauritiana). These values were higher than those reported for fish: 1– 2 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 0.6–1.7 mg kg1 in fish species from the Black Sea (Tuzen 2009), 0.1– 1.5 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009), and 0.3– 2.2 mg kg1 in fish species from the Black Sea (Mendil et al. 2010). Cr is considered an essential trace element. The amount of Cr in the diet is of great importance as Cr is involved in insulin function and lipid metabolism (Bratakos et al. 2002). In the present study, the concentrations of Cr in all sea cucumbers were significantly higher than the AI. Therefore, sea cucumbers are an excellent source of Cr. The Ni levels of sea cucumbers ranged from 0.3 (S. hermanni and S. chloronotus) to 5.1 mg kg1 (B. argus).
These values were similar to those reported for fish: 1.9–5.7 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 1.1–3.6 mg kg1 in fish species from the Black Sea (Tuzen 2009), 0.1– 1.7 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009), and 1.1– 10.2 mg kg1 in fish species from the river (Mendil et al. 2010). There is no information about DRI/AI for Ni levels in the diet set by the USDA. The World Health Organization (WHO) (1994) recommends 0.1–0.3 mg Ni for the daily intake. Therefore, T. ananas, H. fuscogilva, H. fuscopunctata, H. mexicana, A. mauritiana and B. argus are good sources of Ni. The concentrations of contaminants in each sea cucumber were compared with the maximum allowed level (ML) and action level (AL); the results are presented in Table 3. The minimum and maximum As levels observed were 1.1 mg kg1 in H. fuscogilva and 6.1 mg kg1 in H. mexicana. These values were similar to those reported for clams: 2.6–2.9 mg kg1 in Chamelea gallina and 1.7–3.5 mg kg1 in Donax trunculus (Ozden et al. 2009). Moreover, the contents of As in sea cucumbers were lower than those reported for crab: 16–49 mg kg1 in C. pagurus (Barrento et al. 2009b) and lobsters: 11 mg kg1 in H. americanus, 17 mg kg1 in H. gammarus (Barrento et al. 2008). However, the As levels in sea cucumbers were higher than those reported for fish: 0.1–0.3 mg kg1 in fish species from the Black Sea (Tuzen 2009). Although As is a known carcinogen in humans, causing lung, liver, skin and bladder cancer (Kapaj et al. 2006), As from seafood is mainly available in the organic form as the non-toxic arsenobetaine (97–99%), while As in the inorganic form (the most toxic) can damage DNA and cause cancer (Food Standards Agency (FSA) 2004). In the present study, the As concentrations in sea cucumbers were significantly below the AL.
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Food Additives and Contaminants: Part B The Cd concentrations in sea cucumbers ranged from 0.03 to 0.06 mg kg1. These values were similar to those reported for muscle of crab: 0.01–0.02 mg kg1 in C. pagurus (Barrento et al. 2009b), and muscle of lobsters: 0.02 mg kg1 in H. americanus and 0.02 mg kg1 in H. gammarus (Barrento et al. 2008). In general, the Cd values in sea cucumbers were significantly lower than those reported for fish: 0.45– 0.9 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 0.1–0.35 mg kg1 in fish species from the Black Sea (Tuzen 2009), 0.01– 0.39 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009), 0.18– 0.35 mg kg1 in fish species from the Black Sea (Mendil et al. 2010), 0.05–0.63 mg kg1 in fish species from the Eastern Mediterranean (Ersoy and Celik 2010), 0.11–0.75 mg kg1 in fish species from the river (Mendil et al. 2010) and for clams: 0.2–0.43 mg kg1 in C. gallina, 0.02–0.16 mg kg1 in D. trunculus (Ozden et al. 2009). Moreover, the previous studies showed that Cd was mostly accumulated in the hepatopancreas of crustaceans (Barrento et al. 2008, 2009b). Cd is a non-essential element in foods and natural water, Cd exerts a variety of toxic effects, including nephrotoxicity, osteoporosis, neurotoxicity, carcinogenicity, genotoxicity, teratogenicity, endocrine disruptions and reproductive effects (European Food Safety Authority (EFSA) 2004). In the present study, the Cd levels in sea cucumbers were significantly lower than the ML. The Hg values of 11 sea cucumbers were blow the detection limit (0.01 mg kg1). In humans, Hg is toxic to the developing foetus and is considered a possible carcinogen (Ikem and Egilla 2008). Hg is a known human toxicant and the primary sources of mercury contamination in man are through eating fish (EmamiKhansari et al. 2005). In previous studies, the Hg concentrations in fish, crab, lobsters and clams were below the legal limit (Barrento et al. 2008, 2009b; Ozden et al. 2009; Tuzen 2009). In the present study, the Hg contents in sea cucumbers were significantly below the ML. The Pb concentrations in sea cucumbers ranged from 0.11 (A. mauritiana) to 0.69 mg kg1 (H. fuscopunctata). These results were similar to those reported for fish: 0.33–0.93 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 0.28– 0.87 mg kg1 in fish species from the Black Sea (Tuzen 2009), 0.21–1.28 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009), 0.28–0.64 mg kg1 in fish species from the Black Sea (Mendil et al. 2010), 0.1–0.56 mg kg1 in fish species from the river (Mendil et al. 2010), 0.11– 0.76 mg kg1 in fish species from the Eastern Mediterranean (Ersoy and Celik 2010), and for clams: 0.16–1.34 mg kg1 in C. gallina, 0.29– 1.32 mg kg1 in D. trunculus (Ozden et al. 2009).
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Conclusions The present study highlights and provides new information on the elemental composition of 11 sea cucumber species. Considering the daily intake recommendations, sea cucumbers are good sources of Na, Cl, Mg, Ca, Fe, Cu, Se, and Cr. Trace element levels in analysed sea cucumber species were acceptable to human consumption at nutritional and toxicological levels. Future studies should evaluate the mineral composition of other sea cucumber species with relevance for human consumption.
Acknowledgements This work was supported by the National Key Technologies R&D Program (Grant Number 2009BAB44B02); the Science and Technology Program of Guangdong Province (Grant Numbers 2009B091300155, 2007A020300007-15 and A200899E02, A200901E01) and Guangxi Province (Grant Number 0815006-2).
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Nutritional quality and safety of European perch (Perca fluviatilis) from three lakes of Central Italy. Food Chem. 100:482–490. Ozden O, Erkan N, Deval MC. 2009. Trace mineral profiles of the bivalve species Chamelea gallina and Donax trunculus. Food Chem. 113:222–226. Turkmen M, Turkmen A, Tepe Y, Ates A, Gokkus K. 2009. Determination of metals in fish species from the Aegean and Mediterranean seas. Food Chem. 113: 233–237. Turkmen M, Turkmen A, Tepe Y, Tore Y, Ates A. 2008. Determination of metal contaminations in sea foods from Marmara, Aegean and Mediterranean seas: twelve fish species. Food Chem. 108:794–800. Tuzen M. 2009. Toxic and essential trace elemental contents in fish species from the Black Sea, Turkey. Food Chem Toxicol. 47:1785–1790. Uluozlu OD, Tuzen M, Mendil D, Soylak M. 2007. Trace metal content in nine species of fish from the Black and Aegean seas, Turkey. Food Chem. 104:835–840. Uthicke S. 1999. Sediment bioturbation and impact of feeding activity of Holothuria (Halodeima) atra and Stichopus chloronotus, two sediment feeding holothurians, at Lizard Island, Great Barrier Reef. Bull Mar Sci. 64:129–141. Uthicke S. 2001. Nutrient regeneration by abundant coral reef holothurians. J Exp Mar Biol Ecol. 265:153–170. Visnjic-Jeftic Z, Jaric I, Jovanovic L, Skoric S, SmederevacLalic M, Nikcevic M, Lenhardt M. 2010. Heavy metal and trace element accumulation in muscle, liver and gills of the Pontic shad (Alosa immaculata Bennet 1835) from the Danube River (Serbia). Microc. 95:341–344. Walker CH, Hopkin SP, Sibly RM, Peakall DB. 2001. Principles of ecotoxicology. 2nd ed. London (UK): Taylor & Francis. World Health Organization (WHO). 1994. Quality directive of potable water. 2nd ed. Geneva (Switzerland): WHO; p. 197. Yanar Y, Clelik M. 2006. Seasonal amino acid profiles and mineral contents of green tiger shrimp (Penaeus semisulcatus De Haan, 1844) and speckled shrimp (Metapenaeus monoceros Fabricus, 1789) from the Eastern Mediterranean. Food Chem. 94:33–36. Yilmaz AB, Yilmaz L. 2007. Influences of sex and seasons on levels of heavy metals in tissues of green tiger shrimp (Penaeus semisulcatus de Hann, 1844). Food Chem. 101:1664–1669. Zhong Y, Khan MA, Shahidi F. 2007. Compositional characteristics and antioxidant properties of fresh and processed sea cucumber (Cucumaria frondosa). J Agric Food Chem. 55:1188–1192.
Food Additives & Contaminants: Part B: Surveillance Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tfab20
Elemental composition of commercial sea cucumbers (holothurians) J. Wen
a b
& C. Hu
a
a
Key Laboratory of Marine Bio-resources Sustainable Utilization (LMB), Key Laboratory of Applied Marine Biology of Guangdong Province and The Chinese Academy of Sciences (LAMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China b
Department of Biology, Zhanjiang Normal University, Zhanjiang 524048, China Published online: 25 Nov 2010.
To cite this article: J. Wen & C. Hu (2010) Elemental composition of commercial sea cucumbers (holothurians), Food Additives & Contaminants: Part B: Surveillance, 3:4, 246-252, DOI: 10.1080/19393210.2010.520340 To link to this article: http://dx.doi.org/10.1080/19393210.2010.520340
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Food Additives and Contaminants: Part B Vol. 3, No. 4, December 2010, 246–252
VIEW DATASET Elemental composition of commercial sea cucumbers (holothurians) J. Wenab and C. Hua* a
Key Laboratory of Marine Bio-resources Sustainable Utilization (LMB), Key Laboratory of Applied Marine Biology of Guangdong Province and The Chinese Academy of Sciences (LAMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China; bDepartment of Biology, Zhanjiang Normal University, Zhanjiang 524048, China
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(Received 24 July 2010; final version received 30 August 2010) Toxic and essential elements in 11 different sea cucumber species were determined and compared with daily intake recommendations and maximum allowed levels. The contents of macro-elements contents in dried sea cucumber samples were found to be 25,000–152,000 mg kg–1 for Na, 4000–8600 mg kg1 for Mg, 1100–5200 mg kg1 for K, 15,000–68,000 mg kg1 and 36,300–251,000 mg kg1 for Cl. Trace element concentrations in dried sea cucumber samples were found to be 11–100 mg kg1 for Zn, 41–660 mg kg1 for Fe, 3–74 mg kg1 for Cu, 1.1–16 mg kg1 for Mn, 1.4–3.7 mg kg1 for Se, 1.1–9.6 mg kg1 for Cr, and 0.3–5.1 mg kg1 for Ni. All sea cucumber species were rich sources of Na, Cl, Mg, Ca, Fe, Cu, Se and Cr for human consumption. Regarding contaminants, As, Cd and Pb concentrations in dried sea cucumbers were in the ranges of 1.1–6.1, 0.03–0.06 and 0.11–0.69 mg kg1, respectively. Moreover, Hg values of 11 sea cucumbers were below the detection limit (0.01 mg kg1). Keywords: animal products; meat; metals
Introduction Sea cucumbers (also called holothurians) are an enigmatic and diverse group of echinoderms. They are slowmoving invertebrates that can live on sand, mud, rock and reef flats, often related with seaweeds, coral and sea grasses. Most sea cucumbers are detritivores, which is a key role within the marine ecosystem, as they conduct functions including nutrient recycling (Uthicke 2001) and bioturbation (Uthicke 1999). As a kind of seafood, sea cucumbers have a high nutritional value due to their high-protein, low-fat content, amino acid and fatty acid profiles, and they have been regarded as a traditional delicacy, medicine and aphrodisiac in Asia over many centuries. The main use for sea cucumbers as food is for the consumption of the body wall, mostly as a dried product known as ‘beche-de-mer’. Once caught, sea cucumbers are gutted, boiled, and salted and dried (Bruckner 2005). Depending on the conversion factor used for the dry/ wet weight of sea cucumbers, it is possible to infer that the combined catches for the Asia and Pacific regions are in the order of 20,000–40,000 tonnes year1. Sea cucumber species are commercially exploited as food with most of them comprising tropical and sub-tropical species from the families Holothuriidae and
*Corresponding author. Email: [email protected] ISSN 1939–3210 print/ISSN 1939–3229 online ß 2010 Taylor & Francis DOI: 10.1080/19393210.2010.520340 http://www.informaworld.com
Stichopodidae, including the genuses Holothuria, Actinopyga, Bohadschia and Stichopus (Food and Agricultural Organization (FAO) 2008). Essential elements (e.g. Na, Mg, Cl, K, Ca, Mn, Fe, Cu, Zn, Se and Cr) play important roles in biological systems. On the other hand, environmental contaminants (e.g. As, Cd, Hg and Pb) are a major concern in aquatic environments because they are toxic, even in trace amounts. In recent years, attention has been focused on the determination of elements in seafood due to the nutritional benefits of essential elements and toxicological concerns related to contaminants. In the last decade, the essential and toxic elements of fish, clams and crustaceans have been investigated worldwide (Yilmaz and Yilmaz 2007; Barrento et al. 2008; Turkmen et al. 2008, 2009; Mohapatra et al. 2009; Ozden et al. 2009; Tuzen 2009; Mendil et al. 2010; Ersoy and Celik 2010). However, information on the essential and toxic elements of sea cucumber species in food products is lacking. In this context, the aim of this paper was to quantify the essential elements and contaminants contents in the dried products of 11 sea cucumber species, and to compare such values with the daily intake recommendations and maximum limit levels.
Food Additives and Contaminants: Part B Materials and methods
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Sampling Samples of dried Stichopus herrmanni (curryfish), Stichopus chloronotus (greenfish), Thelenota ananas (prickly redfish), Thelenota anax (amberfish), Holothuria scabra (sandfish), Holothuria mexicana (donkey dungfish), Holothuria fuscogilva (white teatfish), Holothuria fuscopunctata (elephant trunkfish), Actinopyga mauritiana (surf redfish), Actinopyga caerulea (blackfish) and Bohadschia argus (tigerfish) products were purchased from a local retail market and supermarket in Guangzhou, China. There were 30 individuals per sample, each sample divided into three groups (ten individuals per group). The samples were ground using a grinder into a fine powder. The ground portions were kept in a plastic bag pending analysis. From each group 100 g powder were used in each analysis discussed below.
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the concentration of elements per 100 g serving portion was calculated and compared with the recommended intake and limits set by international authorities. The average intakes of the essential elements Na, Cl, K, Ca, Mn and Cr were compared with the daily adequate intakes (AI); Mg, Fe, Cu, Zn and Se were compared with the daily dietary reference intake (DRI); and Na, Cl, Ca, Mn, Fe, Cu, Zn and Se were compared with the daily tolerable upper intake levels (UL). AI, DRI and UL were set by the US Department of Agriculture (USDA) for adult females and males aged between 19 and 50 years. The contaminants Cd and Hg were compared with the maximum allowed level (ML) set by the European Commission; As was evaluated in terms of the action level (AL; similar in meaning to the ML) set by the US Food and Drug Administration (USFDA).
Statistical analysis Elemental analyses Element analyses were performed in the China National Analytical Center, Guangzhou. The element content of samples was pre-treated according to the GB/T 5009.12-2003 in China. Each sample was placed in a Teflon digestion vessel with 7 ml of concentrated (65%) nitric acid (HNO3) and 1 ml of 30% hydrogen peroxide (H2O2). The sample in the vessel containing concentrated nitric acid was then subjected to a microwave programme as follows: 25–200 C for 10 min at 1000 W and 200 C for 10 min at 1000 W. Digests were finally made up with deionised water to 25 ml in acid-washed standard flasks. A blank digest was carried out in the same way. Na, Mg, K, Ca, Zn, Cu and Fe were determined by inductively coupled plasma atomic emission spectrometry (ICP-AES) (SPECTRO CIROSCCD) according to the JY/T 0151996 in China. Mn, Se, Cr, Ni, As, Pb and Cd were also measured by inductively coupled plasma mass spectrometry (ICP-MS) (Agilent 7500a) according to the Pharmacopoeia of the People’s Republic of China (2005 edn), Pt 1, Appx XI D in China. Hg was measured by a Zeeman mercury spectrometer (RA915þ) according to the GB/T 15337-2008 in China. Cl was measured by an automatic potentiometric titrator (Metrohm 751 GPD Tirino) according to the GB/T 9695.8-2008 in China. The element standard solutions used for calibration were prepared by diluting stock solutions of 1000 mg l1 of each element supplied from Sigma (St Louis, MO, USA). Element concentrations were calculated on a mg kg1 dry weight basis.
Nutritional quality and potential risks for consumers To evaluate the elemental nutritional quality and potential consumption hazards of sea cucumbers,
All analyses were repeated four times. Results are expressed as means standard deviation (SD), and one-way analysis of variance (ANOVA) was carried out using a statistical analysis system (SPSS Version 12). Differences in the concentration of nutritional elements between species were tested with ANOVA followed by a multiple-comparison test (Tukey HSD). Differences were considered to be significant at p 5 0.05.
Results and discussion The average macro-elements of each sea cucumber are shown in Table 1. Eleven sea cucumbers were excellent sources of macro-elements (Na, Cl, Ca and Mg). The dried sea cucumber products had significantly higher concentrations of Na and Cl. There is no doubt that these elements come from salt (NaCl) during the processing of drying the sea cucumbers. Among the 11 sea cucumbers, H. scabra, A. mauritiana and B. argus had significantly lower Na and Cl concentrations than other species. These differences might reflect distinct salt requirements for the processing of each species. Although the concentrations of Na and Cl from all dried sea cucumbers were above the daily tolerable upper intake levels (UL), dried sea cucumbers were rehydrated by soaking, which is required for preparation for cooking (Zhong et al. 2007). Thus, the excess Na and Cl will decrease during the rehydration processing. The Ca concentrations of sea cucumbers were significant higher than edible tissue from other fishery products, including fish (Orban et al. 2007; Ersoy and Celik 2010), crabs (Chen et al. 2007; Barrento et al. 2009a), shrimps (Yanar and Clelik 2006) and lobsters (Barrento et al. 2008). Sea cucumbers have a reduced skeleton of isolated, microscopic
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Table 1. Mean macro-elemental composition (SD) (mg kg–1 dry weight) in sea cucumbers.a
S. hermanni S. chloronotus T. ananas T. anax H. fuscogilva H. fuscopunctata H. scabra H. mexicana A. mauritiana A. caerulea B. argus
Na AI ¼ 15000 UL ¼ 23000
Mg DRI ¼ 4200 UL ¼ NS
K AI ¼ 47000 UL ¼ NS
Ca AI ¼ 10000 UL ¼ 25000
Cl AI ¼ 23000 UL ¼ 36000
112000 28000a 152000 36000a 105000 27000a 140000 32000a 83000 14000b 107000 26000a 35000 6000c 65000 9000b 28000 5000c 153000 36000a 25000 4000c
6200 600b 6400 300b 5700 200b 6600 300b 8000 300a 7800 600a 6200 300b 4000 200c 7000 600b 8600 400a 8300 400a
1800 200b 1900 200b 1300 100c 2200 100b 1100 100c 1100 100c 2400 200b 1800 200b 2700 200b 5200 200a 2000 100b
25000 4000b 26000 4000b 15000 2000c 19000 2000b 20000 3000b 50000 6000a 67000 6000a 68000 6000a 16000 2000c 23000 4000b 40000 3000a
175000 38000b 196000 39000b 172000 29000b 251000 45000a 154000 23000b 173000 27000b 51600 4900c 114000 12000b 43600 4500c 202000 36000b 36300 2700c
Notes: aValues in the same row bearing different letters are significantly different ( p 5 0.05). DRI, daily dietary reference intake; AI, daily adequate intakes; UL, daily tolerable upper intake levels; and NS, have not been set.
ossicles embedded in a pliable body wall (Kerr and Kim 2005). It was reasonable that the dermal finer ossicles of sea cucumbers were the source of Ca, because the main composition of ossicles was CaCO3. Ca is nutritionally very important as it provides rigidity to the skeleton and plays a role in many metabolic processes (Food and Agricultural Organization/World Health Organization (FAO/ WHO) 2002). Although the Ca concentrations of S. chloronotus, H. fuscopunctata, H. scabra, H. mexicana and B. argus were above the UL, urinary Ca rises very slowly with intake (slope of 5–10%) and the risk of kidney stones from dietary hypercalciuria must therefore be negligible (FAO/WHO 2002). The concentrations of K varied from 1100 to 5200 mg kg1. These results were similar to those reported for fishes (Ersoy and Celik 2010), crabs (Barrento et al. 2009a), shrimps (Yanar and Clelik 2006) and lobsters (Barrento et al. 2008). Concentrations of seven trace elements were studied from the 11 sea cucumbers (Table 2). Mean Zn concentrations of sea cucumbers ranged from 11 (H. fuscogilva) to 100 mg kg1 (B. argus). This result was similar to those reported for fish: 35.4–106 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 38.8–93.4 mg kg1 in fish species from the Black Sea (Tuzen 2009), 66 mg kg1 in Alosa immaculate (Visnjic-Jeftic et al. 2010), 17.8 mg kg1 in Mulus barbatus ponticus and 25.7 mg kg1 in Trachurus trachurus (Mendil et al. 2010), 11.6–63.5 mg kg1 in fish species from the river (Mendil et al. 2010), 8.1–98.5 mg kg1 in fish species from the Eastern Mediterranean (Ersoy and Celik 2010); for crabs: 47–69.9 mg kg1 in Callinectes sapidus, 37.2–46.8 mg kg1 in Portunus pelagicus (Gokodlu and Yerlikaya 2003), 33–91 mg kg1 in Eriocheir sinensis (Chen et al. 2007), 16–90 mg kg1 in Cancer
pagurus (Barrento et al. 2009a); and for lobsters: 26 mg kg1 in Homarus gammarus and 29 mg kg1 in Homarus americanus (Barrento et al. 2008). The Zn contents of sea cucumbers were higher than those reported in the fish Pagrus pagrus (0.61 mg kg1; Miniadis-Meimaroglou et al. 2007) and fish Perca fluviatilis (5.8–7.4 mg kg1; Orban et al. 2007). The Zn values in the present study were lower than those reported as 288–322 mg kg1 in the crab Scylla serrata (Mohapatra et al. 2009). Zn plays an essential role in a number of biological processes involved in growth and development. It is an essential component of several enzymes participating in the synthesis and degradation of carbohydrates, lipids, proteins and nucleic acids. Additionally, this element has also an essential role in the process of gene expression, particularly in polynucleotide transcription (FAO/WHO 2002). Fish, fruit and greenleaf vegetables are considered to be poor sources of Zn (510 mg kg1), whilst lean meat, cereals and legumes are rich Zn sources (25–50 compared with 11–100 mg kg1 in 11 sea cucumbers) (FAO/ WHO 2002). Zn levels in analysed sea cucumbers were found to be lower than the UL (40 mg day1). The result indicated that the consumption of 100 g of the examined sea cucumbers covers a satisfactory percentage of the human diet. The average Fe concentrations of sea cucumbers were different among species. The lowest and highest Fe levels in sea cucumber species were found to be 41 mg kg1 in A. caerulea and 660 mg kg1 in A. mauritiana. The previous studies showed that the Fe concentrations of fish were varied among species: 68.6–163 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 36.2–145 mg kg1 in fish species from the Black Sea (Tuzen 2009), 9.2–136 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009),
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Table 2. Mean trace elemental composition (SD) (mg kg–1 dry weight) in the sea cucumbers.a
S. hermanni S. chloronotus T. ananas T. anax H. fuscogilva H. fuscopunctata H. scabra H. mexicana A. mauritiana A. caerulea B. argus
Zn DRI ¼ 110 UL ¼ 400
Fe DRI ¼ 180 UL ¼ NS
Cu DRI ¼ 9 UL ¼ 100
Mn AI ¼ 23 UL ¼ 110
Se DRI ¼ 0.55 UL ¼ 4
Cr AI ¼ 0.35 UL ¼ NS
Ni DRI ¼ NS UL ¼ 10
33 3.0c 16 2.0d 46 5.0b 28 2.0c 11 2.0d 25 2.0c 77 6.0a 16 2.0d 57 3.0b 20 1.0c 100 19a
94 27c 80 23c 210 39b 200 30b 250 36b 100 20c 130 19c 190 29b 660 36a 41 6.0d 330 41b
3.0 1.0d 3.0 1.0d 44 3.0b 4.0 1.0d 57 5.0b 74 9.0a 18 3.0c 30 2.0b 14 2.0c 4.0 1.0d 18 3.0c
9.1 0.4b 2.2 0.2d 16 1.6a 10 0.9b 9.4 0.3b 12 0.6b 1.4 0.1d 1.6 0.2d 9.2 0.5b 1.1 0.1d 3.7 0.1c
1.7 0.2b 1.4 0.2b 3.7 1.0a 2.5 0.3b 2.6 0.3b 2.1 0.2b 2.4 0.2b 3.5 0.6a 0.9 0.1c 3.2 0.9a 2.4 0.2b
1.6 0.2c 1.5 0.1c 2.7 0.3c 1.5 0.1c 1.3 0.1c 5.5 0.5b 1.1 0.1c 2.2 0.2c 9.6 0.9a 1.3 0.1c 4.9 0.6b
0.3 0.1c 0.3 0.1c 2.5 0.6a 0.7 0.2c 1.5 0.5b 3.0 0.7a 0.6 0.2c 1.1 0.3b 4.2 0.9a 0.5 0.1c 5.1 1.0a
Notes: aValues in the same row bearing different letters are significantly different ( p 5 0.05). DRI, daily dietary reference intake; AI, daily adequate intakes; UL, daily tolerable upper intake levels; and NS, have not been set.
9.6–107.2 mg kg1 in fish species from the Black Sea (Mendil et al. 2010), 6.5–116 mg kg1 in fish species from the river (Mendil et al. 2010), and 26.8– 453 mg kg1 in fish species from the Eastern Mediterranean (Ersoy and Celik 2010). In general, the concentration levels of Fe in sea cucumbers were higher than those reported in crabs (4.5–6.8 mg kg1 in P. pelagicus, 10.4–11.3 mg kg1 in C. sapidus; Gokodlu and Yerlikaya 2003; and 2.2–4.3 mg kg1 in C. pagurus; Barrento et al. 2009a), shrimps (13.6–16.3 mg kg1; Yanar and Clelik 2006) and lobster (18–23 mg kg1; Barrento et al. 2008). Fe has several vital functions in humans, such as carrying oxygen to tissues by red blood cell haemoglobin, as a transport medium for electrons within cells, and as part of important enzyme systems in various tissues (FAO/WHO 2002). Among 11 sea cucumber species, the Fe concentrations of T. ananas, T. anax, H. fuscogilva, H. mexicana, A. mauritiana and B. argus were above the DRI (18 mg day1). Therefore, the six sea cucumber species are excellent source of Fe. The mean Cu concentrations of sea cucumbers ranged from 3 (S. hermanni and S. chloronotus) to 74 mg kg1 (H. fuscopunctata). Among the 11 sea cucumber species, the Cu contents of S. hermanni, S. chloronotus, T. anax, H. scabra, A. mauritiana, A. caerulea and B. argus (ranging from 3 to 18 mg kg1) were similar to those reported for the muscle of crabs: 14.9–20.8 mg kg1 in P. pelagicus (Gokodlu and Yerlikaya 2003), 16 mg kg1 in E. sinensis (Chen et al. 2007), 6.7–10 mg kg1 in C. pagurus (Barrento et al. 2009a); and muscle of lobsters: 9.6 mg kg1 in H. gammarus and 10 mg kg1 in H. americanus (Barrento et al. 2008). However, the Cu values of sea cucumbers were higher than fish: 0.7– 1.8 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 0.7–2.8 mg kg1 in fish
species from the Black Sea (Tuzen 2009), 0.5– 7.1 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009), 1.4– 1.9 mg kg1 in fish species from the Black Sea (Mendil et al. 2010), and 1.0–2.5 mg kg1 in fish species from the river (Mendil et al. 2010). Cu is found in several enzymes, including the cytochrome c oxidase and the superoxide dismutase, and is used for biological electron transport (Walker et al. 2001). The concentrations of T. ananas, H. fuscogilva, H. fuscopunctata, H. scabra, H. mexicana, A. mauritiana and B. argus were reached the DRI and are below the UL. Therefore, the seven sea cucumber species are excellent source of Cu. Mn is one of vital important essential trace element. It is not only a structural component of some enzymes, but also triggers the actions of some enzymes. The concentrations of Mn in sea cucumber species ranged from 1.1 (A. caerulea) to 16 mg kg1 (T. ananas). The Mn values of sea cucumbers were similar to those reported for fish: 1.3–7.4 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 2.8– 9.1 mg kg1 in fish species from the Black Sea (Tuzen 2009a), 0.4–8.7 mg kg1 in fish species from the Black Sea (Mendil et al. 2010), and 1.0–9.4 mg kg1 in fish species from the river (Mendil et al. 2010). Moreover, the Mn contents of sea cucumbers were higher than crabs: 0.6–1.6 mg kg1 in P. pelagicus (Gokodlu and Yerlikaya 2003), 0.9 mg kg1 in E. sinensis (Chen et al. 2007), 0.2–0.3 mg kg1 in C. pagurus (Barrento et al. 2009a); and lobsters: 0.4 mg kg1 in H. gammarus and 0.6 mg kg1 in H. americanus (Barrento et al. 2008). Among the 11 sea cucumber species, T. ananas and H. fuscopunctata are good sources of Mn. The Se concentrations of sea cucumbers ranged from 1.4 (S. chloronotus) to 3.7 mg kg1 (T. ananas). These values were higher than those reported for fish
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Table 3. Mean contaminant composition (standard deviation) (mg kg1 dry weight) in the sea cucumbersa.
S. hermanni S. chloronotus T. ananas T. anax H. fuscogilva H. fuscopunctata H. scabra H. mexicana A. mauritiana A. caerulea B. argus
As AL ¼ 76
Cd ML ¼ 0.5
Hg ML ¼ 0.5
Pb ML ¼ NS
2.5 0.1b 1.7 0.1b 5.1 0.2a 2.8 0.1b 1.1 0.1c 2.0 0.1b 3.8 0.1b 6.1 0.2a 2.1 0.1b 3.3 0.1b 3.2 0.1b
0.03 0.01a 0.06 0.01a 0.03 0.01a 0.04 0.01a 0.04 0.01a 0.04 0.01a 0.03 0.01a 0.03 0.01a 0.05 0.01a 0.06 0.01a 0.03 0.01a
BDL BDL BDL BDL BDL BDL BDL BDL BDL BDL BDL
0.52 0.03a 0.12 0.01c 0.55 0.03a 0.25 0.02b 0.56 0.03a 0.69 0.06a 0.13 0.01c 0.56 0.03a 0.11 0.01c 0.15 0.01c 0.13 0.01c
Notes: aValues in the same row bearing different letters are significantly different ( p 5 0.05). AL, action level; ML, maximum allowed level; BDL, blow detection limit; and NS, have not been set.
(0.2–0.9 mg kg1 in fish species from the Black Sea; Tuzen 2009a), crab (0.7–1.1 mg kg1 in C. pagurus; Barrento et al. 2009a) and lobsters (0.6 mg kg1 in H. gammarus and 0.9 mg kg1 in H. americanus; Barrento et al. 2008). Se is recognised as an essential micronutrient in animal and humans. The previous study has reported the Se-protective action, especially selenite, on many toxicological effects of Cd and Hg (Early et al. 1992). Se is also implicated in the protection of body tissues against oxidative stress, the maintenance of defences against infection, and modulation of growth and development (FAO/WHO 2002). Worldwide, Se availability in sediments and live organisms shows great variability due to distinct environmental conditions and agricultural practices (FAO/WHO 2002). Thus, as a benthonic organism, sea cucumbers are rich in Se. In the present study, the concentrations of Se in all 11 sea cucumbers were significantly higher than the DRI and are below the UL. Sea cucumbers are therefore an excellent source of Se. Cr levels in analysed sea cucumbers ranged from 1.1 (H. scabra) to 9.6 mg kg1 (A. mauritiana). These values were higher than those reported for fish: 1– 2 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 0.6–1.7 mg kg1 in fish species from the Black Sea (Tuzen 2009), 0.1– 1.5 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009), and 0.3– 2.2 mg kg1 in fish species from the Black Sea (Mendil et al. 2010). Cr is considered an essential trace element. The amount of Cr in the diet is of great importance as Cr is involved in insulin function and lipid metabolism (Bratakos et al. 2002). In the present study, the concentrations of Cr in all sea cucumbers were significantly higher than the AI. Therefore, sea cucumbers are an excellent source of Cr. The Ni levels of sea cucumbers ranged from 0.3 (S. hermanni and S. chloronotus) to 5.1 mg kg1 (B. argus).
These values were similar to those reported for fish: 1.9–5.7 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 1.1–3.6 mg kg1 in fish species from the Black Sea (Tuzen 2009), 0.1– 1.7 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009), and 1.1– 10.2 mg kg1 in fish species from the river (Mendil et al. 2010). There is no information about DRI/AI for Ni levels in the diet set by the USDA. The World Health Organization (WHO) (1994) recommends 0.1–0.3 mg Ni for the daily intake. Therefore, T. ananas, H. fuscogilva, H. fuscopunctata, H. mexicana, A. mauritiana and B. argus are good sources of Ni. The concentrations of contaminants in each sea cucumber were compared with the maximum allowed level (ML) and action level (AL); the results are presented in Table 3. The minimum and maximum As levels observed were 1.1 mg kg1 in H. fuscogilva and 6.1 mg kg1 in H. mexicana. These values were similar to those reported for clams: 2.6–2.9 mg kg1 in Chamelea gallina and 1.7–3.5 mg kg1 in Donax trunculus (Ozden et al. 2009). Moreover, the contents of As in sea cucumbers were lower than those reported for crab: 16–49 mg kg1 in C. pagurus (Barrento et al. 2009b) and lobsters: 11 mg kg1 in H. americanus, 17 mg kg1 in H. gammarus (Barrento et al. 2008). However, the As levels in sea cucumbers were higher than those reported for fish: 0.1–0.3 mg kg1 in fish species from the Black Sea (Tuzen 2009). Although As is a known carcinogen in humans, causing lung, liver, skin and bladder cancer (Kapaj et al. 2006), As from seafood is mainly available in the organic form as the non-toxic arsenobetaine (97–99%), while As in the inorganic form (the most toxic) can damage DNA and cause cancer (Food Standards Agency (FSA) 2004). In the present study, the As concentrations in sea cucumbers were significantly below the AL.
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Food Additives and Contaminants: Part B The Cd concentrations in sea cucumbers ranged from 0.03 to 0.06 mg kg1. These values were similar to those reported for muscle of crab: 0.01–0.02 mg kg1 in C. pagurus (Barrento et al. 2009b), and muscle of lobsters: 0.02 mg kg1 in H. americanus and 0.02 mg kg1 in H. gammarus (Barrento et al. 2008). In general, the Cd values in sea cucumbers were significantly lower than those reported for fish: 0.45– 0.9 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 0.1–0.35 mg kg1 in fish species from the Black Sea (Tuzen 2009), 0.01– 0.39 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009), 0.18– 0.35 mg kg1 in fish species from the Black Sea (Mendil et al. 2010), 0.05–0.63 mg kg1 in fish species from the Eastern Mediterranean (Ersoy and Celik 2010), 0.11–0.75 mg kg1 in fish species from the river (Mendil et al. 2010) and for clams: 0.2–0.43 mg kg1 in C. gallina, 0.02–0.16 mg kg1 in D. trunculus (Ozden et al. 2009). Moreover, the previous studies showed that Cd was mostly accumulated in the hepatopancreas of crustaceans (Barrento et al. 2008, 2009b). Cd is a non-essential element in foods and natural water, Cd exerts a variety of toxic effects, including nephrotoxicity, osteoporosis, neurotoxicity, carcinogenicity, genotoxicity, teratogenicity, endocrine disruptions and reproductive effects (European Food Safety Authority (EFSA) 2004). In the present study, the Cd levels in sea cucumbers were significantly lower than the ML. The Hg values of 11 sea cucumbers were blow the detection limit (0.01 mg kg1). In humans, Hg is toxic to the developing foetus and is considered a possible carcinogen (Ikem and Egilla 2008). Hg is a known human toxicant and the primary sources of mercury contamination in man are through eating fish (EmamiKhansari et al. 2005). In previous studies, the Hg concentrations in fish, crab, lobsters and clams were below the legal limit (Barrento et al. 2008, 2009b; Ozden et al. 2009; Tuzen 2009). In the present study, the Hg contents in sea cucumbers were significantly below the ML. The Pb concentrations in sea cucumbers ranged from 0.11 (A. mauritiana) to 0.69 mg kg1 (H. fuscopunctata). These results were similar to those reported for fish: 0.33–0.93 mg kg1 in fish species from the Black and Aegean seas (Uluozlu et al. 2007), 0.28– 0.87 mg kg1 in fish species from the Black Sea (Tuzen 2009), 0.21–1.28 mg kg1 in fish species from the Aegean and Mediterranean seas (Turkmen et al. 2009), 0.28–0.64 mg kg1 in fish species from the Black Sea (Mendil et al. 2010), 0.1–0.56 mg kg1 in fish species from the river (Mendil et al. 2010), 0.11– 0.76 mg kg1 in fish species from the Eastern Mediterranean (Ersoy and Celik 2010), and for clams: 0.16–1.34 mg kg1 in C. gallina, 0.29– 1.32 mg kg1 in D. trunculus (Ozden et al. 2009).
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Conclusions The present study highlights and provides new information on the elemental composition of 11 sea cucumber species. Considering the daily intake recommendations, sea cucumbers are good sources of Na, Cl, Mg, Ca, Fe, Cu, Se, and Cr. Trace element levels in analysed sea cucumber species were acceptable to human consumption at nutritional and toxicological levels. Future studies should evaluate the mineral composition of other sea cucumber species with relevance for human consumption.
Acknowledgements This work was supported by the National Key Technologies R&D Program (Grant Number 2009BAB44B02); the Science and Technology Program of Guangdong Province (Grant Numbers 2009B091300155, 2007A020300007-15 and A200899E02, A200901E01) and Guangxi Province (Grant Number 0815006-2).
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