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The antihyperlipidemic effect of alginate-free residue from sea tangle in hyperlipidemic rats

The antihyperlipidemic effect of alginate-free residue from sea tangle in hyperlipidemic rats Background: In order to assess the high value-added use of the alginate-free residue of sea tangle, an animal study was performed to evaluate the functional activities and key compounds present. In the animal study, sea tangle and the alginate-free residue demonstrated good anti-hyperlipidemic and anti-arteriosclerotic abilities. Results: The functional compounds in the alginate-free residue of the sea tangle were effectively extracted by supercritical fluid extraction (SFE). The optimum extraction temperature and pressure were 40 °C and 6500 psi (M1) in the SFE, a better method in comparison to the conditions of 70 °C and 4500 psi (M2), respectively. The anti- atherosclerotic effects of the alginate-free residue of sea tangle (M1, M2) were investigated in Sprague-Dawley rats treated with poloxamer 407, Triton WR 1339, corn oil, and a high-fat diet. The M1 fraction reduced the serum lipid levels with greater efficacy than the M2 fraction. In the hyperlipidemic rats, treatment with M1 decreased the serum triglyceride (TG), total cholesterol (TC), and low-density lipoprotein-cholesterol (LDL-C) levels when compared to the levels in normal rats. Conclusion: Our results demonstrated that the alginate-free residue of sea tangle reduces serum TC, TG, and LDL- C. These results suggest that the alginate-free residue of sea tangle contains physiologically active components, such as fucosterol, that may exert beneficial effects in the prevention of atherosclerosis. Keywords: Antihyperlipidemic, Fucosterol, Saccharina japonica, Sea tangle Background factors in the initiation and progression of atherosclerotic A number of seaweed species are consumed as food in disease (Goldstein et al., 1973;Harrisonetal., 2003). Hyper- several countries and documented as drugs in traditional cholesterolemia is characterized by an increase in serum Chinese medicine. Fucoidan extracted from L. japonica lipids such as TC, low-density lipoprotein cholesterol (LDL- is an antioxidant, with the fatty acid composition of n–3 C), and TG (Levine et al., 1995). Hyperlipidemia mainly fatty acids, polysaccharides, vitamins, minerals and trace demonstrates increased levels of total cholesterol (TC), TG, elements (Jeong et al., 1993), and minor compounds and LDL-C, along with a decrease in the high-density such as sterols. Saccharina japonica is also well known lipoprotein-cholesterol (HDL-C). Studies have indicated the for several biological activities, including antioxidant, potential of synthetic and natural sources that could regulate anti-mutagenic, and antibacterial activities (Okai et al., plasma TC and TG levels in coronary atherosclerosis (Ghule 1993; Wang et al., 2006; Park et al., 2009). et al., 2009). Recently, many studies have reported on prospective nat- The sea tangle is often used as a functional food or ural resources regulating the serum cholesterol and trigly- alginate extraction material in Korea and Japan. The ceride (TG) levels (Ghule et al., 2006;Lemhadriet al., 2006). alginate-free residue of sea tangle is discarded as waste. Hypercholesterolemia and hyperlipidemia are important risk For the purpose of high value-added use of the alginate- free residue of sea tangle, we investigated the anti- * Correspondence: daesung@mabik.re.kr hyperlipidemic and anti-atherosclerotic effects of the National Marine Biodiversity Institute of Korea (MABIK), Seocheon, alginate-free residue from sea tangle. Chungcheongnam-do 325-902, Republic of Korea Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Yim et al. Fisheries and Aquatic Sciences (2019) 22:27 Page 2 of 6 Methods normal and high-fat diet are shown in Table 1. The Materials and chemicals high-fat-diet–treated rats were orally administered the The sea tangle (Saccharina japonica) was obtained from a test substance for the last week, with the high-fat diets local supplier (Gangneung, Gangwon-do, Korea) in March fed daily for 6 weeks. 2007. Poloxamer-407 (Pluronic F-127) and corn oil were purchased from Sigma (St. Louis, MO, USA). TC (Choleste- Extraction of feces lipids zyme-V), TG (Triglyzyme-V), and high-density lipoprotein- Based on the method of Folch et al. (1957), the lipids cholesterol (HDL-C; HDL-C555) were assayed using com- were extracted by homogenization of the feces with 2:1 mercially available kits (Asan Pharm. Co., Ltd., Korea). chloroform-methanol (v/v), followed by centrifugation. The lipids were extracted based on the dry weight of the Preparation of samples feces and assayed for TC and TG concentration using a The functional compounds (M1 and M2) in the alginate- standard enzymatic assay kit (Asan Pharm., Korea). free residue of sea tangle were effectively extracted by supercritical fluid extraction (SFX 3560, Lincoln, USA). Glucose analysis Supercritical CO was used as a solvent and extraction The levels of TG, TC, and HDL-C were determined by was performed using 1.0 g sea tangle in a 10-mL extractor. enzymatic colorimetric methods using commercial kits The extraction was performed for 20 min with a fluid flow (Shinyang Chemical Co., Busan, Korea). The concentra- rate of 1.0 mL/min, measured at the pump head. The ex- tion of LDL-C was calculated using the following equa- traction was performed at 40 °C and 6500 psi in the sam- tion (Friedwald et al., 1972). ple cartridge for 10 min, followed by extraction through LDL-C = TC–HDL-C–(TG/5) the cartridge at 70 °C. The extracted sample was collected in collection vial with ethanol. Identification of M1 with HPLC High-performance liquid chromatograph (HPLC, Hitachi, Animals and treatments Tokyo, Japan) system was performed using a Lichrospher Sprague-Dawley male rats weighing 130–150 g were ob- RP-18e column (8 × 250 mm, Merck). The mobile phase tained from the Dae-han Biolink Co., Ltd. (Chungbuk, Re- used was methanol/acetonitrile (7:3, v/v) at a flow rate of public of Korea), maintained under constant conditions 1.0 mL/min, and detection was performed at 450 nm and (temperature 20 ± 2 °C, humidity 40–60%, light 12-h 210 nm by a diode array detector (L7455 type, Hitachi). cycle) and acclimatized for 1 week. The rats had free ac- The amounts of M1 fractions were quantified from their cess to drinking water, with the feed prepared according peak area by the use of a standard curve identified with to the recommendations of the American Institute of Nu- fucosterol. trition (AIN-76). After the animals were fed the AIN-76 diets, 50 or 100 mg (lipid solution/kg of body weight in Statistical analysis 5% Tween 80) of the alginate-free residue extracted from All results are presented as the mean ± SD. Data were sea tangle powder was orally administered, once a day for evaluated by one-way ANOVA using SPSS (IBM SPSS, 2 weeks. Following this period, the rats were fasted for 24 h and killed and dissected under CO anesthesia. All ani- Table 1 Composition of the normal and high-fat diet (Unit: mal experiments were approved by the University of g/100 g) Kyungsung Animal Care and Use Committee. Ingredients Normal diet High-fat diet Casein 20 29 Experimental procedures Corn starch 60 10 The poloxamer-407 hyperlipidemic diet model was de- Sugar 0.0 10 termined according to the method described by Wout et al. (1992). The rats were administered a 300 mg/kg Lard 0.0 35 dose of poloxamer 407 intraperitoneally, prepared by Corn oil 9.0 5.0 combining the agent with saline solution. Cellulose 5.0 5.0 The Triton WR-1339 hyperlipidemic diet model was per- AIN76 mineral mixture 3.5 3.5 formed according to the method described by Kusama AIN76 vitamin mixture 1.0 1.0 et al. (1998). Triton WR-1339 (200 mg/kg) was injected Cholesterol 1.0 1.0 into the tail vein after a fasting period of 16 h. After indu- cing hyperlipidemia, the animals were anesthetized with the DL-methionine 0.3 0.3 CO gas and blood was gathered for analysis 18 h later. 2 Choline 0.2 0.2 According to Duhault et al. (1976), we administered AIN76 mixture: Nutritional Biochemicals, ICN Life Science Group, corn oil in the diet at 3 g/kg. The compositions of the Cleveland, Ohio Yim et al. Fisheries and Aquatic Sciences (2019) 22:27 Page 3 of 6 Table 2 Effect of M1and M2 on the serum lipid levels in Table 4 Effect of M1 on the serum triglyceride, total cholesterol poloxamer-407 injected rats and low-density lipoprotein-cholesterol (LDL-C) levels in Triton WR 1339-induced hyperlipidemic rats Treatment Dose Triglyceride Total cholesterol Treatment Dose Triglyceride Total cholesterol LDL-C mg/kg mg/dL d c mg/kg mg/dL Normal 80.6 ± 8.46 66.5 ± 9.49 d c c a a Normal 98.4 ± 15.9 79.6 ± 9.36 18.2 ± 2.43 Poloxamer-407 1101.6 ± 63.7 770.3 ± 48.8 a a a c b Control 736.5 ± 30.8 191.4 ± 14.5 67.3 ± 8.57 M1 100 881.3 ± 52.2 620.9 ± 33.6 b b b b a M1 50 639.5 ± 45.7 167.0 ± 10.8 53.7 ± 4.53 M2 100 996.5 ± 70.3 728.6 ± 43.1 c b b 100 424.8 ± 38.5 150.9 ± 7.53 49.0 ± 5.07 Values represent mean ± S.D. (n = 8). Values sharing the same column superscript letter are not significantly different from each other (P < 0.05) by Values represent mean ± S.D. (n=9). Values sharing the same column Duncan’s multiple range test superscript letter are not significantly different from each other (P < 0.05) by Duncan’s multiple range test Armonk, NY, USA), after which the differences between were reduced in the M1-treated groups compared with the means values were assessed using Duncan’smultiple control rats; however, no dose-dependent differences range test. Results were considered statistically significant were observed between M1 and M2. at P <0.05. The effect of M1 on 30% corn oil-induced hyperlipidemia Results Table 5 shows the serum lipid levels following the oral The effect of M1 and M2 on poloxamer 407-induced administration of M1 50 and 100 mg/kg body weight. hyperlipidemia The serum lipid levels such as TG and TC were remark- We assessed the effect of the oral administration of M1 ably increased in the control rats induced corn oil; how- and M2 100 mg/kg of body weight, once a day for 2 ever, the administration of M1 significantly reduced the weeks, on the serum lipid levels in poloxamer 407- serum TG and TC levels. induced hyperlipidemic rats. Serum TG and TC levels were reduced by M1 and M2 when compared to the The effect of M1 on high fat diet-induced hyperlipidemia control rats, in poloxamer 407-induced hyperlipidemic The effects of M1 on the serum lipid levels of rats fed a rats (Table 2). M1 demonstrated a more potent effect on high-fat diet are shown in Table 6. The rats fed a high- the serum lipid levels than the M2 fraction. Hence, we fat diet reported significantly increased levels of serum proceeded to assess if M1 possessed a dose-dependent of TG, TC, and LDL-C compared to the normal rats. effect. The administration of the M1 at a dose of 50 and The serum lipid levels including TG, TC, and LDL-C 100 mg/kg body weight significantly reduced serum lipid were significantly reduced by M1 100 mg/kg, with no levels when compared to the control rats (Table 3). reduction observed in the serum lipid levels of the con- trol rats (Table 6). The abdominal fat pad weights in the The effect of M1 on Triton WR 1339-induced normal and diet-induced obesity rats fed with M1 were hyperlipidemia also assessed. The weights of the retroperitoneal WAT, Rats with hyperlipidemia induced by Triton WR 1339 epididymal WAT, and total abdominal WAT per body demonstrated remarkably high serum levels of TG, TC, weight of rats were significantly lower in the diet- and LDL-C. However, the administration of the M1 at induced obesity rats treated with M1 100 mg/kg body doses of 50 and 100 mg/kg body weight significantly weight than the control rats (Table 7). The fecal con- reduced the TG levels in the hyperlipidemic rats as com- tents of the diet-induced obesity rats were not altered pared to the control rats (Table 4). The TC and LDL-C when compared to dose-dependent of M1. The rats fed Table 3 Effect of M1 on the serum lipid levels in poloxamer- Table 5 Effect of M1 on the serum triglyceride and total 407 treated rats cholesterol levels in 30% corn oil-induced hyperlipidemic rats Treatment Dose Triglyceride Total cholesterol Treatment Dose Triglyceride Total cholesterol mg/kg mg/dL mg/kg mg/dL d c c c Normal 81.7 ± 9.53 69.8 ± 8.56 Normal 86.8 ± 10.5 73.5 ± 8.56 a a a a Poloxamer-407 1207.8 ± 100.5 800.6 ± 50.4 Control 230.7 ± 19.7 98.8 ± 7.79 b a b a M1 50 937.5 ± 87.9 740.6 ± 47.8 M1 50 197.6 ± 20.3 91.6 ± 9.66 c a b b 100 741.6 ± 94.7 531.2 ± 63.2 100 172.9 ± 11.1 86.7 ± 5.24 Values represent mean ± S.D. (n=9). Values sharing the same column Values represent mean ± S.D. (n=9). Values sharing the same column superscript letter are not significantly different from each other (P < 0.05) by superscript letter are not significantly different from each other (P < 0.05) by Duncan’s multiple range test Duncan’s multiple range test Yim et al. Fisheries and Aquatic Sciences (2019) 22:27 Page 4 of 6 Table 6 Serum lipid contents of the normal and diet-induced Table 8 Feces lipid contents of the normal and diet-induced obesity rats fed with M1 for 2 weeks obesity rats fed with M1 for 2 weeks Treatment Dose Triglyceride Total cholesterol LDL-C Treatment Dose Dry Total lipid Triglyceride Total weight cholesterol mg/kg mg/dL mg/ g/day mg/g c c c Normal 76.9 ± 4.80 66.9 ± 4.57 20.6 ± 4.26 kg a a a Control 121.3 ± 11.3 119.0 ± 3.56 76.5 ± 10.5 Normal 2.46 ± 66.4 ± 16.4 ± 3.9 ± 0.79 a c c a,b a a 0.17 6.83 1.36 M1 50 111.6 ± 9.53 115.2 ± 5.27 65.2 ± 5.28 b b b Control 1.01 ± 133.2 ± 17.8 ± 15.6 ± 2.31 100 97.7 ± 5.23 106.3 ± 3.11 51.4 ± 3.26 b b c 0.11 5.87 1.58 Values represent mean ± S.D. (n=9). Values sharing the same column a,b superscript letter are not significantly different from each other (P < 0.05) by M1 50 0.93 ± 140.5 ± 21.3 ± 18.6 ± 2.46 b b b Duncan’s multiple range test 0.15 7.66 2.17 100 0.85 ± 153.9 ± 26.8 ± 20.5 ± 1.47 b a a the M1 100 mg/kg of body weight diet decreased of total 0.13 6.05 1.90 lipid, TG and TC (Table 8). The rats fed M1 100 mg/kg Values represent mean ± S.D. (n=9). Values sharing the same column reported lower blood leptin and insulin levels than the superscript letter are not significantly different from each other (P < 0.05) by Duncan’s multiple range test control rats (Table 9). rats (Nigon et al., 2001; Ara et al., 2002; Yamada et al., Identification of compounds 2003; Megalli et al., 2005; Jeong et al., 2010). According To find a key functional anti-hyperlipidemic compound to these studies, lowering serum TC and LDL-C levels in M1, the properties were compared with the reference plays an important role in reducing the risk of develop- substance after separation using the HPLC (data not ing atherosclerosis. shown). The results demonstrated fucosterol as the key In addition, the diet-induced obesity rats treated with functional compound (Fig. 1). M1 reported decreased abdominal fat weight compared to the control rats. These results suggest that the M1 fraction Discussion effects obesity by reducing the abdominal fat weight in Hyperlipidemia, obesity, and diabetes mellitus are chronic obese rats. We also investigated the total lipid, TG, and diseases associated with serious complications that may TC levels in the fecal contents of the control and diet- consequently increase the risk of atherosclerosis. Thus, induced obesity rats fed with M1. The M1-treated rats re- regulating the serum cholesterol levels is important, as in- ported increased fecal content of the total lipid, TG, and creased serum levels of TC and LDL-C are the significant TC levels. This data indicated that M1 lowered the serum determinants in the development of atherosclerosis (Jeong lipid through the increased excretion of total lipid, TG, et al., 2010). and TC from the body. Hence, it was concluded that M1 In the present study, we investigated the effects of the demonstrated hypolipidemic activity in rats. Moreover, alginate residue extracted from sea tangle on the serum lowering the serum cholesterol level is crucial for the pre- lipid profile of hyperlipidemic and diet-induced obesity vention of cardiovascular diseases (Hideomi et al., 2005). rats. The results demonstrated that M1 administration M1 treatments also exerted anti-hyperlipidemic effects by in the hyperlipidemic rats significantly decreased the regulating the serum lipid levels in rats with induced serum TC, TG, and LDL-C levels. Previous studies have hyperlipidemia. HPLC was performed to confirm the pres- reported the hypolipidemic effects of edible seaweeds, ence of functional components in the M1 fraction, and dietary fiber, plant sterols, and herbal extracts, as indi- the identification of fucosterol in the M1 fraction was cated by decreased serum TC, TG, and LDL-C levels on confirmed by the comparison of retention times with the Table 7 Abdominal fat pad weights in the normal and diet- Table 9 Serum leptin and insulin levels in the normal and diet- induced obesity rats fed with M1 for 2 weeks induced obesity rats fed with M1 for 2 weeks Treatment Dose Retroperitoneal Epididymal Total abdominal Treatment Dose Leptin Insulin mg/kg g mg/kg mg/dL c c c c b Normal 6.44 ± 0.37 7.82 ± 0.46 14.26 ± 0.97 Normal 8.76 ± 0.47 3.56 ± 0.19 a a a a a Control 10.58 ± 0.83 12.06 ± 0.53 22.56 ± 1.54 Control 26.25 ± 6.43 4.16 ± 0.30 a,b a,b a,b a a M1 50 9.53 ± 0.46 11.17 ± 0.50 20.70 ± 0.86 M1 50 24.83 ± 3.29 4.06 ± 0.28 b b b b a,b 100 8.69 ± 0.50 10.53 ± 0.49 19.22 ± 0.95 100 16.55 ± 3.10 3.97 ± 0.21 Values represent mean ± S.D. (n=9). Values sharing the same column Values represent mean ± S.D. (n=9). Values sharing the same column superscript letter are not significantly different from each other (P < 0.05) by superscript letter are not significantly different from each other (P < 0.05) by Duncan’s multiple range test Duncan’s multiple range test Yim et al. Fisheries and Aquatic Sciences (2019) 22:27 Page 5 of 6 Ethics approval and consent to participate Animal experiments were performed according to the institutional guidelines for the care and the use of laboratory animals, and the protocol was approved by the Animal Ethics Committee of Kyungsung University. Consent for publication Not applicable. Competing interests The authors declare that they have no competing interests. Author details National Marine Biodiversity Institute of Korea (MABIK), Seocheon, Chungcheongnam-do 325-902, Republic of Korea. Department of Food Processing and Distribution, Gangneung-Wonju National University, 210-702, Fig. 1 Structure of fucosterol Gangneung 25457, Republic of Korea. Received: 27 September 2019 Accepted: 12 November 2019 reference standard. In previous studies, fucosterol, isolated from marine algae Pelvetia siliquosa,has been investigated for anti-oxidant and anti-diabetic activities (Lee et al., References 2003;Lee et al., 2004). Furthermore, many studies have re- Ara J, Sultana V, Qasim R, Ahmad VU. Hypolipidemic activity of seaweed from Karachi Coast. Phytother Res. 2002;16:479–83. ported that among the serum lipids, LDL-C is the most Aviram M. Modified forms of low density lipoprotein and atherosclerosis. dangerous, as the oxidation of LDL leads to its increased Atherosclerosis. 1993;98:1–9. infiltration in the arterial walls (Aviram, 1993). Therefore, Duhault J, Boulanger M, Beregi L, Sicot N, Bouvier F. A new type of hyperlipidemic agent comparative assay in rats. Atherosclerosis. 1976;23:63–72. reducing the oxidation of LDL-C is essential due to the Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and presumed involvement in the development of atheroscler- purification of total lipids from animal tissues. J Biol Chem. 1957;226:497–509. otic disease. Friedwald WT, Levy RL, Fedreicson DS. Estimation of the concentration of low- density lipoprotein cholesterol in plasma, without was of the preparative ultracentrifuge. Clin Chem. 1972;18:499–506. Ghule BV, Ghante MH, Saoji AN, Yeole PG. Hypolipidemic and Conclusions antihyperlipidemic effects of Lagenaria siceraria Stand. Fruit extracts. Our results demonstrated that the alginate-free residue Indian J Exp Biol. 2006;44:905–9. of sea tangle reduces serum levels of TC, TG, and LDL- Ghule BV, Ghante MH, Saoji AN, Yeole PG. Antihyperlipidemic effect of the methanolic extract from Lagenaria siceraria Stand. Fruit in hyperlipidemic C. These results suggest that the alginate-free residue of rats. J Ethnopharmacol. 2009;124:333–7. sea tangle contains physiologically active components, Goldstein JL, Schroot HG, Hazzard WR, Bierman EL, Motulsky AG. Hyperlipidemia such as fucosterol, that may exert beneficial effects in in coronary heart disease 11: genetic analysis of lipid levels in 176 families and delineation of a new inherited disorder, combined hyperlipidemia. J Clin the prevention of atherosclerosis. Invest. 1973;52:1544–68. Harrison D, Griendling KK, Landmesser U, Hornig B, Drexler H. Role of oxidative stress in atherosclerosis. Am J Cardiol. 2003;91:7A–11A. Abbreviations Hideomi A, Makoto K, Daniel AC, Haruka O, Takaaki H. Effect of a seaweed HDL-C: High-density lipoprotein-cholesterol; LDL-C: Low-density mixture on serum lipid level and platelet aggregation in rats. Fish Sci. 2005; lipoproteincholesterol; SFE: Supercritical fluid extraction; TC: Total cholesterol; 71:1160–6. TG: Triglycerides; TSO: Trans-stilbene oxide Jeong BY, Cho DM, Moon SK, Pyeun JH. Quality factors and functional components in the edible seaweeds - I. Distribution on n-3 fatty acids in 10 Acknowledgements species of seaweeds by their habitats. J Korean Soc Food Sci Nutr. 1993;22: This work was supported by the study for the establishment of the marine 612–28. natural products library, funded by the National Marine Biodiversity Institute Jeong SC, Jeong YT, Yang BK, Islam R, Koyyalamudi SR, Pang G, Cho KY, Song CH. of Korea (2019M00700). White button mushroom (Agaricus bisporus) lowers blood glucose and cholesterol levels in diabetic and hypercholesterolemic rats. Nutr Res. 2010; 30:49–56. Authors’ contributions Kusama H, Nishiyama M, Ikeda S. Pharmacological investigation of bezafibrate a MJY carried out the hypolipidemic activity and drafted the manuscript. GC hypolopodemic agent. Effects of bezafibrate on normal and experimental carried out the glucose and cholesterol analysis. JML identified fucosterol as hyperlipidemia in rats. Nihon Yakurigaku Zasshi. 1998;92:175–80. the key functional compound. SYC participated in the design of the study Lee S, Lee YS, Jung SH, Kang SS, Shin KH. Anti-oxidant activities of fucosterol and helped to draft the manuscript. DSL designed the study and completed from the marine algae Pelvetia siliquosa. Arch Pharm Res. 2003;26:719–22. the manuscript. All authors read and approved the final manuscript. Lee YS, Shin KH, Kim BK, Lee S. Anti-diabetic activities of fucosterol from Pelvetia siliquosa. Arch Pharm Res. 2004;27:1120–2. Lemhadri A, Hajji L, Michel JB, Eddouks MJ. Cholesterol and triglycerides lowering Funding activities of caraway fruits in normal and streptozotocin diabetic rats. J This work was supported by the study for the establishment of the marine Ethnopharmacol. 2006;106:321–6. natural products library, funded by the National Marine Biodiversity Institute Levine GN, Keaney JF Jr, Vita JA. Cholesterol reduction in cardiovascular disease. of Korea (2019M00700). Clinical benefits and possible mechanisms. N Engl J Med. 1995;332:512–21. Megalli S, Aktan F, Davies NM, Roufogalis BD. Phytopreventative anti- Availability of data and materials hyperlipidemic effects of Gynostemma pentaphyllum in rats. J Pharm Pharm Not applicable. Sci. 2005;8:507–15. Yim et al. Fisheries and Aquatic Sciences (2019) 22:27 Page 6 of 6 Nigon F, Serfaty-Lacrosniere C, Beucler I, Beucler I, Chauvois D, Neveu C, Giral P, Giral P, Chapman MJ, Bruckert E. Plant sterol-enriched margarine lowers plasma LDL in hyperlipidemic subjects with low cholesterol intake: effect of fibrate treatment. Clin Chem Lab Med. 2001;39:634–40. Okai Y, Higashi-okai K, Nakamura S. Identification of heterogenous antimutagenic activities in the extract of edible brown seaweeds, Laminaria japonica (Makonbu) and Undaria pinnatifida (Wakame) by the umu gene expression system in Salmonella typhimurium (TA1535/pSK1002). 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The antihyperlipidemic effect of alginate-free residue from sea tangle in hyperlipidemic rats

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Abstract

Background: In order to assess the high value-added use of the alginate-free residue of sea tangle, an animal study was performed to evaluate the functional activities and key compounds present. In the animal study, sea tangle and the alginate-free residue demonstrated good anti-hyperlipidemic and anti-arteriosclerotic abilities. Results: The functional compounds in the alginate-free residue of the sea tangle were effectively extracted by supercritical fluid extraction (SFE). The optimum extraction temperature and pressure were 40 °C and 6500 psi (M1) in the SFE, a better method in comparison to the conditions of 70 °C and 4500 psi (M2), respectively. The anti- atherosclerotic effects of the alginate-free residue of sea tangle (M1, M2) were investigated in Sprague-Dawley rats treated with poloxamer 407, Triton WR 1339, corn oil, and a high-fat diet. The M1 fraction reduced the serum lipid levels with greater efficacy than the M2 fraction. In the hyperlipidemic rats, treatment with M1 decreased the serum triglyceride (TG), total cholesterol (TC), and low-density lipoprotein-cholesterol (LDL-C) levels when compared to the levels in normal rats. Conclusion: Our results demonstrated that the alginate-free residue of sea tangle reduces serum TC, TG, and LDL- C. These results suggest that the alginate-free residue of sea tangle contains physiologically active components, such as fucosterol, that may exert beneficial effects in the prevention of atherosclerosis. Keywords: Antihyperlipidemic, Fucosterol, Saccharina japonica, Sea tangle Background factors in the initiation and progression of atherosclerotic A number of seaweed species are consumed as food in disease (Goldstein et al., 1973;Harrisonetal., 2003). Hyper- several countries and documented as drugs in traditional cholesterolemia is characterized by an increase in serum Chinese medicine. Fucoidan extracted from L. japonica lipids such as TC, low-density lipoprotein cholesterol (LDL- is an antioxidant, with the fatty acid composition of n–3 C), and TG (Levine et al., 1995). Hyperlipidemia mainly fatty acids, polysaccharides, vitamins, minerals and trace demonstrates increased levels of total cholesterol (TC), TG, elements (Jeong et al., 1993), and minor compounds and LDL-C, along with a decrease in the high-density such as sterols. Saccharina japonica is also well known lipoprotein-cholesterol (HDL-C). Studies have indicated the for several biological activities, including antioxidant, potential of synthetic and natural sources that could regulate anti-mutagenic, and antibacterial activities (Okai et al., plasma TC and TG levels in coronary atherosclerosis (Ghule 1993; Wang et al., 2006; Park et al., 2009). et al., 2009). Recently, many studies have reported on prospective nat- The sea tangle is often used as a functional food or ural resources regulating the serum cholesterol and trigly- alginate extraction material in Korea and Japan. The ceride (TG) levels (Ghule et al., 2006;Lemhadriet al., 2006). alginate-free residue of sea tangle is discarded as waste. Hypercholesterolemia and hyperlipidemia are important risk For the purpose of high value-added use of the alginate- free residue of sea tangle, we investigated the anti- * Correspondence: daesung@mabik.re.kr hyperlipidemic and anti-atherosclerotic effects of the National Marine Biodiversity Institute of Korea (MABIK), Seocheon, alginate-free residue from sea tangle. Chungcheongnam-do 325-902, Republic of Korea Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Yim et al. Fisheries and Aquatic Sciences (2019) 22:27 Page 2 of 6 Methods normal and high-fat diet are shown in Table 1. The Materials and chemicals high-fat-diet–treated rats were orally administered the The sea tangle (Saccharina japonica) was obtained from a test substance for the last week, with the high-fat diets local supplier (Gangneung, Gangwon-do, Korea) in March fed daily for 6 weeks. 2007. Poloxamer-407 (Pluronic F-127) and corn oil were purchased from Sigma (St. Louis, MO, USA). TC (Choleste- Extraction of feces lipids zyme-V), TG (Triglyzyme-V), and high-density lipoprotein- Based on the method of Folch et al. (1957), the lipids cholesterol (HDL-C; HDL-C555) were assayed using com- were extracted by homogenization of the feces with 2:1 mercially available kits (Asan Pharm. Co., Ltd., Korea). chloroform-methanol (v/v), followed by centrifugation. The lipids were extracted based on the dry weight of the Preparation of samples feces and assayed for TC and TG concentration using a The functional compounds (M1 and M2) in the alginate- standard enzymatic assay kit (Asan Pharm., Korea). free residue of sea tangle were effectively extracted by supercritical fluid extraction (SFX 3560, Lincoln, USA). Glucose analysis Supercritical CO was used as a solvent and extraction The levels of TG, TC, and HDL-C were determined by was performed using 1.0 g sea tangle in a 10-mL extractor. enzymatic colorimetric methods using commercial kits The extraction was performed for 20 min with a fluid flow (Shinyang Chemical Co., Busan, Korea). The concentra- rate of 1.0 mL/min, measured at the pump head. The ex- tion of LDL-C was calculated using the following equa- traction was performed at 40 °C and 6500 psi in the sam- tion (Friedwald et al., 1972). ple cartridge for 10 min, followed by extraction through LDL-C = TC–HDL-C–(TG/5) the cartridge at 70 °C. The extracted sample was collected in collection vial with ethanol. Identification of M1 with HPLC High-performance liquid chromatograph (HPLC, Hitachi, Animals and treatments Tokyo, Japan) system was performed using a Lichrospher Sprague-Dawley male rats weighing 130–150 g were ob- RP-18e column (8 × 250 mm, Merck). The mobile phase tained from the Dae-han Biolink Co., Ltd. (Chungbuk, Re- used was methanol/acetonitrile (7:3, v/v) at a flow rate of public of Korea), maintained under constant conditions 1.0 mL/min, and detection was performed at 450 nm and (temperature 20 ± 2 °C, humidity 40–60%, light 12-h 210 nm by a diode array detector (L7455 type, Hitachi). cycle) and acclimatized for 1 week. The rats had free ac- The amounts of M1 fractions were quantified from their cess to drinking water, with the feed prepared according peak area by the use of a standard curve identified with to the recommendations of the American Institute of Nu- fucosterol. trition (AIN-76). After the animals were fed the AIN-76 diets, 50 or 100 mg (lipid solution/kg of body weight in Statistical analysis 5% Tween 80) of the alginate-free residue extracted from All results are presented as the mean ± SD. Data were sea tangle powder was orally administered, once a day for evaluated by one-way ANOVA using SPSS (IBM SPSS, 2 weeks. Following this period, the rats were fasted for 24 h and killed and dissected under CO anesthesia. All ani- Table 1 Composition of the normal and high-fat diet (Unit: mal experiments were approved by the University of g/100 g) Kyungsung Animal Care and Use Committee. Ingredients Normal diet High-fat diet Casein 20 29 Experimental procedures Corn starch 60 10 The poloxamer-407 hyperlipidemic diet model was de- Sugar 0.0 10 termined according to the method described by Wout et al. (1992). The rats were administered a 300 mg/kg Lard 0.0 35 dose of poloxamer 407 intraperitoneally, prepared by Corn oil 9.0 5.0 combining the agent with saline solution. Cellulose 5.0 5.0 The Triton WR-1339 hyperlipidemic diet model was per- AIN76 mineral mixture 3.5 3.5 formed according to the method described by Kusama AIN76 vitamin mixture 1.0 1.0 et al. (1998). Triton WR-1339 (200 mg/kg) was injected Cholesterol 1.0 1.0 into the tail vein after a fasting period of 16 h. After indu- cing hyperlipidemia, the animals were anesthetized with the DL-methionine 0.3 0.3 CO gas and blood was gathered for analysis 18 h later. 2 Choline 0.2 0.2 According to Duhault et al. (1976), we administered AIN76 mixture: Nutritional Biochemicals, ICN Life Science Group, corn oil in the diet at 3 g/kg. The compositions of the Cleveland, Ohio Yim et al. Fisheries and Aquatic Sciences (2019) 22:27 Page 3 of 6 Table 2 Effect of M1and M2 on the serum lipid levels in Table 4 Effect of M1 on the serum triglyceride, total cholesterol poloxamer-407 injected rats and low-density lipoprotein-cholesterol (LDL-C) levels in Triton WR 1339-induced hyperlipidemic rats Treatment Dose Triglyceride Total cholesterol Treatment Dose Triglyceride Total cholesterol LDL-C mg/kg mg/dL d c mg/kg mg/dL Normal 80.6 ± 8.46 66.5 ± 9.49 d c c a a Normal 98.4 ± 15.9 79.6 ± 9.36 18.2 ± 2.43 Poloxamer-407 1101.6 ± 63.7 770.3 ± 48.8 a a a c b Control 736.5 ± 30.8 191.4 ± 14.5 67.3 ± 8.57 M1 100 881.3 ± 52.2 620.9 ± 33.6 b b b b a M1 50 639.5 ± 45.7 167.0 ± 10.8 53.7 ± 4.53 M2 100 996.5 ± 70.3 728.6 ± 43.1 c b b 100 424.8 ± 38.5 150.9 ± 7.53 49.0 ± 5.07 Values represent mean ± S.D. (n = 8). Values sharing the same column superscript letter are not significantly different from each other (P < 0.05) by Values represent mean ± S.D. (n=9). Values sharing the same column Duncan’s multiple range test superscript letter are not significantly different from each other (P < 0.05) by Duncan’s multiple range test Armonk, NY, USA), after which the differences between were reduced in the M1-treated groups compared with the means values were assessed using Duncan’smultiple control rats; however, no dose-dependent differences range test. Results were considered statistically significant were observed between M1 and M2. at P <0.05. The effect of M1 on 30% corn oil-induced hyperlipidemia Results Table 5 shows the serum lipid levels following the oral The effect of M1 and M2 on poloxamer 407-induced administration of M1 50 and 100 mg/kg body weight. hyperlipidemia The serum lipid levels such as TG and TC were remark- We assessed the effect of the oral administration of M1 ably increased in the control rats induced corn oil; how- and M2 100 mg/kg of body weight, once a day for 2 ever, the administration of M1 significantly reduced the weeks, on the serum lipid levels in poloxamer 407- serum TG and TC levels. induced hyperlipidemic rats. Serum TG and TC levels were reduced by M1 and M2 when compared to the The effect of M1 on high fat diet-induced hyperlipidemia control rats, in poloxamer 407-induced hyperlipidemic The effects of M1 on the serum lipid levels of rats fed a rats (Table 2). M1 demonstrated a more potent effect on high-fat diet are shown in Table 6. The rats fed a high- the serum lipid levels than the M2 fraction. Hence, we fat diet reported significantly increased levels of serum proceeded to assess if M1 possessed a dose-dependent of TG, TC, and LDL-C compared to the normal rats. effect. The administration of the M1 at a dose of 50 and The serum lipid levels including TG, TC, and LDL-C 100 mg/kg body weight significantly reduced serum lipid were significantly reduced by M1 100 mg/kg, with no levels when compared to the control rats (Table 3). reduction observed in the serum lipid levels of the con- trol rats (Table 6). The abdominal fat pad weights in the The effect of M1 on Triton WR 1339-induced normal and diet-induced obesity rats fed with M1 were hyperlipidemia also assessed. The weights of the retroperitoneal WAT, Rats with hyperlipidemia induced by Triton WR 1339 epididymal WAT, and total abdominal WAT per body demonstrated remarkably high serum levels of TG, TC, weight of rats were significantly lower in the diet- and LDL-C. However, the administration of the M1 at induced obesity rats treated with M1 100 mg/kg body doses of 50 and 100 mg/kg body weight significantly weight than the control rats (Table 7). The fecal con- reduced the TG levels in the hyperlipidemic rats as com- tents of the diet-induced obesity rats were not altered pared to the control rats (Table 4). The TC and LDL-C when compared to dose-dependent of M1. The rats fed Table 3 Effect of M1 on the serum lipid levels in poloxamer- Table 5 Effect of M1 on the serum triglyceride and total 407 treated rats cholesterol levels in 30% corn oil-induced hyperlipidemic rats Treatment Dose Triglyceride Total cholesterol Treatment Dose Triglyceride Total cholesterol mg/kg mg/dL mg/kg mg/dL d c c c Normal 81.7 ± 9.53 69.8 ± 8.56 Normal 86.8 ± 10.5 73.5 ± 8.56 a a a a Poloxamer-407 1207.8 ± 100.5 800.6 ± 50.4 Control 230.7 ± 19.7 98.8 ± 7.79 b a b a M1 50 937.5 ± 87.9 740.6 ± 47.8 M1 50 197.6 ± 20.3 91.6 ± 9.66 c a b b 100 741.6 ± 94.7 531.2 ± 63.2 100 172.9 ± 11.1 86.7 ± 5.24 Values represent mean ± S.D. (n=9). Values sharing the same column Values represent mean ± S.D. (n=9). Values sharing the same column superscript letter are not significantly different from each other (P < 0.05) by superscript letter are not significantly different from each other (P < 0.05) by Duncan’s multiple range test Duncan’s multiple range test Yim et al. Fisheries and Aquatic Sciences (2019) 22:27 Page 4 of 6 Table 6 Serum lipid contents of the normal and diet-induced Table 8 Feces lipid contents of the normal and diet-induced obesity rats fed with M1 for 2 weeks obesity rats fed with M1 for 2 weeks Treatment Dose Triglyceride Total cholesterol LDL-C Treatment Dose Dry Total lipid Triglyceride Total weight cholesterol mg/kg mg/dL mg/ g/day mg/g c c c Normal 76.9 ± 4.80 66.9 ± 4.57 20.6 ± 4.26 kg a a a Control 121.3 ± 11.3 119.0 ± 3.56 76.5 ± 10.5 Normal 2.46 ± 66.4 ± 16.4 ± 3.9 ± 0.79 a c c a,b a a 0.17 6.83 1.36 M1 50 111.6 ± 9.53 115.2 ± 5.27 65.2 ± 5.28 b b b Control 1.01 ± 133.2 ± 17.8 ± 15.6 ± 2.31 100 97.7 ± 5.23 106.3 ± 3.11 51.4 ± 3.26 b b c 0.11 5.87 1.58 Values represent mean ± S.D. (n=9). Values sharing the same column a,b superscript letter are not significantly different from each other (P < 0.05) by M1 50 0.93 ± 140.5 ± 21.3 ± 18.6 ± 2.46 b b b Duncan’s multiple range test 0.15 7.66 2.17 100 0.85 ± 153.9 ± 26.8 ± 20.5 ± 1.47 b a a the M1 100 mg/kg of body weight diet decreased of total 0.13 6.05 1.90 lipid, TG and TC (Table 8). The rats fed M1 100 mg/kg Values represent mean ± S.D. (n=9). Values sharing the same column reported lower blood leptin and insulin levels than the superscript letter are not significantly different from each other (P < 0.05) by Duncan’s multiple range test control rats (Table 9). rats (Nigon et al., 2001; Ara et al., 2002; Yamada et al., Identification of compounds 2003; Megalli et al., 2005; Jeong et al., 2010). According To find a key functional anti-hyperlipidemic compound to these studies, lowering serum TC and LDL-C levels in M1, the properties were compared with the reference plays an important role in reducing the risk of develop- substance after separation using the HPLC (data not ing atherosclerosis. shown). The results demonstrated fucosterol as the key In addition, the diet-induced obesity rats treated with functional compound (Fig. 1). M1 reported decreased abdominal fat weight compared to the control rats. These results suggest that the M1 fraction Discussion effects obesity by reducing the abdominal fat weight in Hyperlipidemia, obesity, and diabetes mellitus are chronic obese rats. We also investigated the total lipid, TG, and diseases associated with serious complications that may TC levels in the fecal contents of the control and diet- consequently increase the risk of atherosclerosis. Thus, induced obesity rats fed with M1. The M1-treated rats re- regulating the serum cholesterol levels is important, as in- ported increased fecal content of the total lipid, TG, and creased serum levels of TC and LDL-C are the significant TC levels. This data indicated that M1 lowered the serum determinants in the development of atherosclerosis (Jeong lipid through the increased excretion of total lipid, TG, et al., 2010). and TC from the body. Hence, it was concluded that M1 In the present study, we investigated the effects of the demonstrated hypolipidemic activity in rats. Moreover, alginate residue extracted from sea tangle on the serum lowering the serum cholesterol level is crucial for the pre- lipid profile of hyperlipidemic and diet-induced obesity vention of cardiovascular diseases (Hideomi et al., 2005). rats. The results demonstrated that M1 administration M1 treatments also exerted anti-hyperlipidemic effects by in the hyperlipidemic rats significantly decreased the regulating the serum lipid levels in rats with induced serum TC, TG, and LDL-C levels. Previous studies have hyperlipidemia. HPLC was performed to confirm the pres- reported the hypolipidemic effects of edible seaweeds, ence of functional components in the M1 fraction, and dietary fiber, plant sterols, and herbal extracts, as indi- the identification of fucosterol in the M1 fraction was cated by decreased serum TC, TG, and LDL-C levels on confirmed by the comparison of retention times with the Table 7 Abdominal fat pad weights in the normal and diet- Table 9 Serum leptin and insulin levels in the normal and diet- induced obesity rats fed with M1 for 2 weeks induced obesity rats fed with M1 for 2 weeks Treatment Dose Retroperitoneal Epididymal Total abdominal Treatment Dose Leptin Insulin mg/kg g mg/kg mg/dL c c c c b Normal 6.44 ± 0.37 7.82 ± 0.46 14.26 ± 0.97 Normal 8.76 ± 0.47 3.56 ± 0.19 a a a a a Control 10.58 ± 0.83 12.06 ± 0.53 22.56 ± 1.54 Control 26.25 ± 6.43 4.16 ± 0.30 a,b a,b a,b a a M1 50 9.53 ± 0.46 11.17 ± 0.50 20.70 ± 0.86 M1 50 24.83 ± 3.29 4.06 ± 0.28 b b b b a,b 100 8.69 ± 0.50 10.53 ± 0.49 19.22 ± 0.95 100 16.55 ± 3.10 3.97 ± 0.21 Values represent mean ± S.D. (n=9). Values sharing the same column Values represent mean ± S.D. (n=9). Values sharing the same column superscript letter are not significantly different from each other (P < 0.05) by superscript letter are not significantly different from each other (P < 0.05) by Duncan’s multiple range test Duncan’s multiple range test Yim et al. Fisheries and Aquatic Sciences (2019) 22:27 Page 5 of 6 Ethics approval and consent to participate Animal experiments were performed according to the institutional guidelines for the care and the use of laboratory animals, and the protocol was approved by the Animal Ethics Committee of Kyungsung University. Consent for publication Not applicable. Competing interests The authors declare that they have no competing interests. Author details National Marine Biodiversity Institute of Korea (MABIK), Seocheon, Chungcheongnam-do 325-902, Republic of Korea. 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Journal

Fisheries and Aquatic Sciences – Springer Journals

Published: Dec 1, 2019

Keywords: Fish & Wildlife Biology & Management; Marine & Freshwater Sciences; Zoology; Animal Ecology

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