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ISSN (Print): 2210-3155
ISSN (Online): 2210-3163

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Research Article

Holothuria arenicola Extract Attenuated Hepatic Steatosis in Splenectomized Rat Fed High Fat Diet

Author(s): Shimaa A. Sadek*, Asmaa E. Farouk, Sohair R. Fahmy and Amel M. Soliman

Volume 12, Issue 3, 2022

Published on: 21 January, 2022

Article ID: e270921196809 Pages: 14

DOI: 10.2174/2210315511666210927122059

Price: $65

Abstract

Background: Non-alcoholic fatty liver disease (NAFLD) is a considerable public health concern due to the excessive dietary consumption of high caloric diet and subsequent obesity. Additionally, splenectomy is considered one of the major common risk factors for NAFLD.

Objective: Regardless of the non-alcoholic fatty liver disease (NAFLD) being the most common chronic disorder, there is no effective cure for it. Therefore, the current study aimed to investigate the efficacy of Holothuria arenicola extract (HaE) on hepatic steatosis in splenectomized (SPX) rats fed High fat diet (HFD).

Methods: Male Wistar rats (n=28) were randomly assigned to four groups: sham rats fed a standard diet, sham rats+ HFD, SPX+HFD and SPX+HFD+HaE. The estimation of hematological and some biochemical parameters, as well as oxidative status, were analyzed.

Results: Oral administration of HaE caused a significant amelioration in all hematological parameters relative to untreated splenectomized rats. Concerning lipid metabolism, HaE treatment caused a pronounced amelioration in lipid metabolism, as indicated by the decreased total cholesterol, triglycerides and LDL-cholesterol contents, as well as the increased HDL- cholesterol level. HaE treatment significantly enhanced hepatic function, as exhibited by the reduction in liver enzyme activities as well as the increase in protein and albumin content. Moreover, HaE could retard the hepatic oxidative stress via a pronounced increase in hepatic GSH content and antioxidant enzyme activities besides decreasing MDA, NO and H2O2 formation.

Conclusion: HaE could be utilized as a potential alternative hepatoprotective remedy via lipid metabolism and oxidative damage attenuation.

Keywords: Hepatic steatosis, Holothuria arenicola, splenectomy, high fat diet, lipid metabolism, oxidative stress.

Graphical Abstract

[1]
Juárez-Hernández, E.; Chávez-Tapia, N.C.; Uribe, M.; Barbero-Becerra, V.J. Role of bioactive fatty acids in nonalcoholic fatty liver disease. Nutr. J., 2016, 15(1), 72.
[http://dx.doi.org/10.1186/s12937-016-0191-8] [PMID: 27485440]
[2]
Pais, R.; Charlotte, F.; Fedchuk, L.; Bedossa, P.; Lebray, P.; Poynard, T.; Ratziu, V. A systematic review of follow-up biopsies reveals disease progression in patients with non-alcoholic fatty liver. J. Hepatol., 2013, 59(3), 550-556.
[http://dx.doi.org/10.1016/j.jhep.2013.04.027] [PMID: 23665288]
[3]
Cicero, A.F.G.; Colletti, A.; Bellentani, S. Nutraceutical approach to non-alcoholic fatty liver disease (NAFLD): The Available clinical evidence. Nutrients, 2018, 10(9), 1153.
[http://dx.doi.org/10.3390/nu10091153] [PMID: 30142943]
[4]
Almeda-Valdes, P.; Altamirano-Barrera, A.; Méndez-Sánchez, N. Insights in non-alcoholic fatty liver disease pathophysiology with lipidomic analyses. Ann. Hepatol., 2015, 14(4), 567-569.
[http://dx.doi.org/10.1016/S1665-2681(19)31182-2] [PMID: 26019047]
[5]
Tsochatzis, E.A.; Papatheodoridis, G.V.; Archimandritis, A.J. Adipokines in nonalcoholic steatohepatitis: from pathogenesis to implications in diagnosis and therapy. Mediators Inflamm., 2009, 2009, 831670.
[http://dx.doi.org/10.1155/2009/831670] [PMID: 19753129]
[6]
Chen, T.; Yuan, F.; Wang, H.; Tian, Y.; He, L.; Shao, Y.; Li, N.; Liu, Z. Perilla oil supplementation ameliorates high-fat/high-cholesterol diet induced non-alcoholic fatty liver disease in rats via enhanced fecal cholesterol and bile acid excretion. BioMed Res. Int., 2016, 2016, 2384561.
[http://dx.doi.org/10.1155/2016/2384561] [PMID: 27642591]
[7]
Borén, J.; Taskinen, M.R.; Olofsson, S.O.; Levin, M. Ectopic lipid storage and insulin resistance: a harmful relationship. J. Intern. Med., 2013, 274(1), 25-40.
[http://dx.doi.org/10.1111/joim.12071] [PMID: 23551521]
[8]
Ito, M.; Suzuki, J.; Tsujioka, S.; Sasaki, M.; Gomori, A.; Shirakura, T.; Hirose, H.; Ito, M.; Ishihara, A.; Iwaasa, H.; Kanatani, A. Longitudinal analysis of murine steatohepatitis model induced by chronic exposure to high-fat diet. Hepatol. Res., 2007, 37(1), 50-57.
[http://dx.doi.org/10.1111/j.1872-034X.2007.00008.x] [PMID: 17300698]
[9]
Wikan, N.; Tocharus, J.; Sivasinprasasn, S.; Kongkaew, A.; Chaichompoo, W.; Suksamrarn, A.; Tocharus, C. Capsaicinoid nonivamide improves nonalcoholic fatty liver disease in rats fed a high-fat diet. J. Pharmacol. Sci., 2020, 143(3), 188-198.
[http://dx.doi.org/10.1016/j.jphs.2020.03.008] [PMID: 32414691]
[10]
Stephenson, K.; Kennedy, L.; Hargrove, L.; Demieville, J.; Thomson, J.; Alpini, G.; Francis, H. Updates on dietary models of non-alcoholic fatty liver disease: Current studies and insights. Gene Expr., 2018, 18(1), 5-17.
[http://dx.doi.org/10.3727/105221617X15093707969658] [PMID: 29096730]
[11]
Paulo, D.N.; Paulo, I.C.; Morais, A.A.; Kalil, M.; Guerra, A.J.; Colnago, G.L.; Faintuch, J. Is splenectomy a dyslipidemic intervention? Experimental response of serum lipids to different diets and operations. Microsurgery, 2009, 29(2), 154-160.
[http://dx.doi.org/10.1002/micr.20568] [PMID: 18942648]
[12]
Rezende, A.B.; Neto, N.N.; Fernandes, L.R.; Ribeiro, A.C.; Alvarez-Leite, J.I.; Teixeira, H.C. Splenectomy increases atherosclerotic lesions in apolipoprotein E deficient mice. J. Surg. Res., 2011, 171(2), e231-e236.
[http://dx.doi.org/10.1016/j.jss.2011.08.010] [PMID: 21962813]
[13]
Inoue, M.; Gotoh, K.; Seike, M.; Masaki, T.; Oribe, J.; Honda, K.; Kakuma, T.; Yoshimatsu, H. Involvement of remnant spleen volume on the progression of steatohepatitis in diet-induced obese rats after a splenectomy. Hepatol. Res., 2012, 42(2), 203-212.
[http://dx.doi.org/10.1111/j.1872-034X.2011.00914.x] [PMID: 22136188]
[14]
Gonçalves, T.B.; Yamaki, V.N.; Feijó, D.H.; Souza, L.E.; Silveira, E.; Brito, M.V.; Petroianu, A. Effects of splenic allograft in lipid profile of non-splenectomized rats: the immune and metabolic role of the “double spleen”. Rev. Col. Bras. Cir., 2014, 41(2), 122-127.
[http://dx.doi.org/10.1590/S0100-69912014000200009] [PMID: 24918726]
[15]
Goldfarb, A.W.; Rachmilewitz, E.A.; Eisenberg, S. Abnormal low and high density lipoproteins in homozygous beta-thalassaemia. Br. J. Haematol., 1991, 79(3), 481-486.
[http://dx.doi.org/10.1111/j.1365-2141.1991.tb08059.x] [PMID: 1751376]
[16]
Fargion, S.; Porzio, M.; Fracanzani, A.L. Nonalcoholic fatty liver disease and vascular disease: state-of-the-art. World J. Gastroenterol., 2014, 20(37), 13306-13324.
[http://dx.doi.org/10.3748/wjg.v20.i37.13306] [PMID: 25309067]
[17]
Sahebkar, A.; Chew, G.T.; Watts, G.F. New peroxisome proliferator-activated receptor agonists: potential treatments for atherogenic dyslipidemia and non-alcoholic fatty liver disease. Expert Opin. Pharmacother., 2014, 15(4), 493-503.
[http://dx.doi.org/10.1517/14656566.2014.876992] [PMID: 24428677]
[18]
Huang, F.; Wang, J.; Yu, F.; Tang, Y.; Ding, G.; Yang, Z.; Sun, Y. Protective effect of Meretrix meretrix oligopeptides on high- fat-diet induced non-alcoholic fatty liver disease in mice. Mar. Drugs, 2018, 16(2), 39.
[http://dx.doi.org/10.3390/md16020039] [PMID: 29360762]
[19]
Pangestuti, R.; Arifin, Z. Medicinal and health benefit effects of functional sea cucumbers. J. Tradit. Complement. Med., 2017, 8(3), 341-351.
[http://dx.doi.org/10.1016/j.jtcme.2017.06.007] [PMID: 29992105]
[20]
Bordbar, S.; Anwar, F.; Saari, N. High-value components and bioactives from sea cucumbers for functional foods- a review. Mar. Drugs, 2011, 9(10), 1761-1805.
[http://dx.doi.org/10.3390/md9101761] [PMID: 22072996]
[21]
Liu, X.; Sun, Z.; Zhang, M.; Meng, X.; Xia, X.; Yuan, W.; Xue, F.; Liu, C. Antioxidant and antihyperlipidemic activities of polysaccharides from sea cucumber Apostichopus japonicus. Carbohydr. Polym., 2012, 90(4), 1664-1670.
[http://dx.doi.org/10.1016/j.carbpol.2012.07.047] [PMID: 22944431]
[22]
Hu, X.Q.; Xu, J.; Xue, Y.; Li, Z.J.; Wang, J.F.; Wang, J.H.; Xue, C.H.; Wang, Y.M. Effects of bioactive components of sea cucumber on the serum, liver lipid profile and lipid absorption. Biosci. Biotechnol. Biochem., 2012, 76(12), 2214-2218.
[http://dx.doi.org/10.1271/bbb.120495] [PMID: 23221720]
[23]
Fahmy, S.R. Holothuria arenicola as promising material for therapeutic drugs. SOJ Pharm. Pharm. Sci., 2018, 5(2), 1-6.
[http://dx.doi.org/10.15226/2374-6866/5/2/00177]
[24]
Fahmy, S.R.; Mohamed, A.S. Holoturia arenicola extract modulates bile duct ligation-induced oxidative stress in rat kidney. Int. J. Clin. Exp. Pathol., 2015, 8(2), 1649-1657.
[PMID: 25973050]
[25]
Yasumoto, T.; Nakamura, K.; Hashimoto, Y. A new saponin holothurin isolated from the sea cucumber Holothuria vagabunda. Agric. Biol. Chem., 1967, 31, 7-10.
[http://dx.doi.org/10.1080/00021369.1967.10858767]
[26]
AOAC.Official methods of analysis of the Association of Official Analytical Chemists, 17th ed; AOAC International: Gaithersburg, MD, 2000.
[27]
Gandhisan, R.; Thamaraichelvan, A. Baburaj. Anti-inflammatory action of Lannea coromandelica by HRBC membrane stabilization. Fitotherapia, 1991, 62, 82-83.
[28]
Wang, Z.; Li, N.; Wang, B.; Lin, J. Nonalcoholic fatty liver disease progression in rats is accelerated by splenic regulation of liver PTEN/AKT. Saudi J. Gastroenterol., 2015, 21(4), 232-238.
[http://dx.doi.org/10.4103/1319-3767.161641] [PMID: 26228367]
[29]
Thrall, M.A.; Weiser, M.G. Haematology. Laboratory Procedures for Veterinary Technicians, 4th ed; Hendrix, C.M., Ed.; Mosby Inc: Missouri, 2002, pp. 29-74.
[30]
Dacie, J.; Lewis, S. Practical haematology, 7th ed; ELBS with Churchill Livingstone: Edinburgh, 1991.
[31]
Burlis, A.; Ashwood, E.R. Tietz Texbook of Clinical Chemistry, 3rd ed; AACC, 1999.
[32]
Henry, R.J.; Chiamori, N.; Golub, O.J.; Berkman, S. Revised spectrophotometric methods for the determination of glutamic oxaloacetic transaminase, glutamic pyruvic transaminase and lactic acid dehydrogenase. Amer J. clin. Path, 1960, 34, 1-398.
[33]
Cancello, R.; Henegar, C.; Viguerie, N.; Taleb, S.; Poitou, C.; Rouault, C.; Coupaye, M.; Pelloux, V.; Hugol, D.; Bouillot, J.L.; Bouloumié, A.; Barbatelli, G.; Cinti, S.; Svensson, P.A.; Barsh, G.S.; Zucker, J.D.; Basdevant, A.; Langin, D.; Clément, K. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes, 2005, 54(8), 2277-2286.
[http://dx.doi.org/10.2337/diabetes.54.8.2277] [PMID: 16046292]
[34]
Garraud, O.; Borhis, G.; Badr, G.; Degrelle, S.; Pozzetto, B.; Cognasse, F.; Richard, Y. Revisiting the B-cell compartment in mouse and humans: more than one B-cell subset exists in the marginal zone and beyond. BMC Immunol., 2012, 13, 63-70.
[http://dx.doi.org/10.1186/1471-2172-13-63] [PMID: 23194300]
[35]
Sengupta, A.; Ghosh, M. Integrity of erythrocytes of hypercholesterolemic and normocholesterolemic rats during ingestion of different structured lipids. Eur. J. Nutr., 2011, 50(6), 411-419.
[http://dx.doi.org/10.1007/s00394-010-0150-7] [PMID: 21127890]
[36]
Benson, T.W.; Weintraub, N.L.; Kim, H.W.; Seigler, N.; Kumar, S.; Pye, J.; Horimatsu, T.; Pellenberg, R.; Stepp, D.W.; Lucas, R.; Bogdanov, V.Y.; Litwin, S.E.; Brittain, J.E.; Harris, R.A. A single high-fat meal provokes pathological erythrocyte remodeling and increases myeloperoxidase levels: implications for acute coronary syndrome. Lab. Invest., 2018, 98(10), 1300-1310.
[http://dx.doi.org/10.1038/s41374-018-0038-3] [PMID: 29572498]
[37]
Hui, D.Y.; Harmony, J.A. Interaction of plasma lipoproteins with erythrocytes. I. Alteration of erythrocyte morphology. Biochim. Biophys. Acta, 1979, 550(3), 407-424.
[http://dx.doi.org/10.1016/0005-2736(79)90145-7] [PMID: 217429]
[38]
Swirski, F.K.; Nahrendorf, M.; Etzrodt, M.; Wildgruber, M.; Cortez-Retamozo, V.; Panizzi, P.; Figueiredo, J.L.; Kohler, R.H.; Chudnovskiy, A.; Waterman, P.; Aikawa, E.; Mempel, T.R.; Libby, P.; Weissleder, R.; Pittet, M.J. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science, 2009, 325(5940), 612-616.
[http://dx.doi.org/10.1126/science.1175202] [PMID: 19644120]
[39]
Li, Y.; Stone, J.R. The impact of splenectomy on human coronary artery atherosclerosis and vascular macrophage distribution. Cardiovasc. Pathol., 2016, 25(6), 453-460.
[http://dx.doi.org/10.1016/j.carpath.2016.08.001] [PMID: 27614166]
[40]
Otogawa, K.; Kinoshita, K.; Fujii, H.; Sakabe, M.; Shiga, R.; Nakatani, K.; Ikeda, K.; Nakajima, Y.; Ikura, Y.; Ueda, M.; Arakawa, T.; Hato, F.; Kawada, N. Erythrophagocytosis by liver macrophages (Kupffer cells) promotes oxidative stress, inflammation, and fibrosis in a rabbit model of steatohepatitis: implications for the pathogenesis of human nonalcoholic steatohepatitis. Am. J. Pathol., 2007, 170(3), 967-980.
[http://dx.doi.org/10.2353/ajpath.2007.060441] [PMID: 17322381]
[41]
Sevmis, M.; Yoyen-Ermis, D.; Aydin, C.; Bilgic, E.; Korkusuz, P.; Uner, A.; Hamaloglu, E.; Esendagli, G.; Karakoc, D. Splenectomy induced leukocytosis promotes intratumoral accumulation of myeloid-derived suppressor cells, angiogenesis and metastasis. Immunol. Invest., 2017, 46(7), 663-676.
[http://dx.doi.org/10.1080/08820139.2017.1360339] [PMID: 28872973]
[42]
Cai, Y.Q.; Zhou, J.; Chen, X.D.; Wang, Y.C.; Wu, Z.; Peng, B. Laparoscopic splenectomy is an effective and safe intervention for hypersplenism secondary to liver cirrhosis. Surg. Endosc., 2011, 25(12), 3791-3797.
[http://dx.doi.org/10.1007/s00464-011-1790-2] [PMID: 21681623]
[43]
Lijnen, P.; Echevaría-Vázquez, D.; Petrov, V. Influence of cholesterol-lowering on plasma membrane lipids and function. Methods Find. Exp. Clin. Pharmacol., 1996, 18(2), 123-136.
[PMID: 8740244]
[44]
Yuniati, R.; Sulardiono, B. Effectivity of Holothuria scabra and Spirulina platensis extract combination as an anti-inflammatory agent measured by carrageenan-induced rat paw edema. Ind. J. Marine Sci., 2020, 25(3), 103-109.
[http://dx.doi.org/10.14710/ik.ijms.25.3.103-109]
[45]
Saravanan, S.; Pari, L. Role of thymol on hyperglycemia and hyperlipidemia in high fat diet-induced type 2 diabetic C57BL/6J mice. Eur. J. Pharmacol., 2015, 761, 279-287.
[http://dx.doi.org/10.1016/j.ejphar.2015.05.034] [PMID: 26007642]
[46]
Kwon, E.Y.; Kim, S.Y.; Choi, M.S. Luteolin-enriched Artichoke leaf extract alleviates the metabolic syndrome in mice with high- fat diet-induced obesity. Nutrients, 2018, 10(8), 979.
[http://dx.doi.org/10.3390/nu10080979] [PMID: 30060507]
[47]
Jensen, V.S.; Hvid, H.; Damgaard, J.; Nygaard, H.; Ingvorsen, C.; Wulff, E.M.; Lykkesfeldt, J.; Fledelius, C. Dietary fat stimulates development of NAFLD more potently than dietary fructose in Sprague-Dawley rats. Diabetol. Metab. Syndr., 2018, 10, 4.
[http://dx.doi.org/10.1186/s13098-018-0307-8] [PMID: 29410708]
[48]
Howard, B.V.; Ruotolo, G.; Robbins, D.C. Obesity and dyslipidemia. Endocrinol. Metab. Clin. North Am., 2003, 32(4), 855-867.
[http://dx.doi.org/10.1016/S0889-8529(03)00073-2] [PMID: 14711065]
[49]
Asai, K.; Kuzuya, M.; Naito, M.; Funaki, C.; Kuzuya, F. Effects of splenectomy on serum lipids and experimental atherosclerosis. Angiology, 1988, 39(6), 497-504.
[http://dx.doi.org/10.1177/000331978803900602] [PMID: 3377269]
[50]
Schmidt, H.H.; Wagner, S.; Manns, M. The spleen as a storage pool in lipid metabolism. Am. J. Gastroenterol., 1997, 92(6), 1072.
[PMID: 9177547]
[51]
Han, B.; Jian, Y.; Xia, X.; Hu, W.; Zhang, L.; Zhou, P. Studying the effects of sea cucumber ovum powder on nonalcoholic fatty liver disease by proteomics techniques in a rat model. Food Funct., 2020, 11(7), 6139-6147.
[http://dx.doi.org/10.1039/D0FO00741B] [PMID: 32573635]
[52]
Meng, J.; Hu, X.; Zhang, T.; Dong, P.; Li, Z.; Xue, C.; Chang, Y.; Wang, Y. Saponin from sea cucumber exhibited more significant effects than ginsenoside on ameliorating high fat diet-induced obesity in C57BL/6 mice. MedChemComm, 2018, 9(4), 725-734.
[http://dx.doi.org/10.1039/C7MD00653E] [PMID: 30108963]
[53]
Han, L.K.; Xu, B.J.; Kimura, Y.; Zheng, Y.N.; Okuda, H. Platycodi radix affects lipid metabolism in mice with high fat diet-induced obesity. J. Nutr., 2000, 130(11), 2760-2764.
[http://dx.doi.org/10.1093/jn/130.11.2760] [PMID: 11053518]
[54]
Reis, P.; Holmberg, K.; Watzke, H.; Leser, M.E.; Miller, R. Lipases at interfaces: a review. Adv. Colloid Interface Sci., 2009, 147-148, 237-250.
[http://dx.doi.org/10.1016/j.cis.2008.06.001] [PMID: 18691682]
[55]
Liu, H.H.; Ko, W.C.; Hu, M.L. Hypolipidemic effect of glycosaminoglycans from the sea cucumber Metriatyla scabra in rats fed a cholesterol-supplemented diet. J. Agric. Food Chem., 2002, 50(12), 3602-3606.
[http://dx.doi.org/10.1021/jf020070k] [PMID: 12033836]
[56]
Lee, L.; Alloosh, M.; Saxena, R.; Van Alstine, W.; Watkins, B.A.; Klaunig, J.E.; Sturek, M.; Chalasani, N. Nutritional model of steatohepatitis and metabolic syndrome in the Ossabaw miniature swine. Hepatology, 2009, 50(1), 56-67.
[http://dx.doi.org/10.1002/hep.22904] [PMID: 19434740]
[57]
Welch-White, V.; Dawkins, N.; Graham, T.; Pace, R. The impact of high fat diets on physiological changes in euthyroid and thyroid altered rats. Lipids Health Dis., 2013, 12, 100.
[http://dx.doi.org/10.1186/1476-511X-12-100] [PMID: 23849139]
[58]
VanWagner, L.B.; Green, R.M. Evaluating elevated bilirubin levels in asymptomatic adults. JAMA, 2015, 313(5), 516-517.
[http://dx.doi.org/10.1001/jama.2014.12835] [PMID: 25647209]
[59]
Ogunlana, O.O.; Ogunlana, O.E.; Ugochukwu, S.K.; Adeyemi, A.O. Assessment of the ameliorative effect of Ruzu herbal bitters on the biochemical and antioxidant abnormalities induced by high fat diet in Wistar rats. Int. J. Pharmacol., 2018, 14, 329-341.
[http://dx.doi.org/10.3923/ijp.2018.329.341]
[60]
Helal, M.G.; Ayoub, S.E.; Elkashefand, W.F.; Ibrahim, T.M. Caffeine affects HFD-induced hepatic steatosis by multifactorial intervention. Hum. Exp. Toxicol., 2018, 37(9), 983-990.
[http://dx.doi.org/10.1177/0960327117747026] [PMID: 29249184]
[61]
Fahmy, S.R.; Hamdi, S.A. Curative effect of the Egyptian marine Erugosquilla massavensis extract on carbon tetrachloride-induced oxidative stress in rat liver and erythrocytes. Eur. Rev. Med. Pharmacol. Sci., 2011, 15(3), 303-312.
[PMID: 21528777]
[62]
Lim, S.S.; Vos, T.; Flaxman, A.D.; Danaei, G.; Shibuya, K.; Adair-Rohani, H.; Amann, M.; Anderson, H.R.; Andrews, K.G.; Aryee, M.; Atkinson, C.; Bacchus, L.J.; Bahalim, A.N.; Balakrishnan, K.; Balmes, J.; Barker-Collo, S.; Baxter, A.; Bell, M.L.; Blore, J.D.; Blyth, F.; Bonner, C.; Borges, G.; Bourne, R.; Boussinesq, M.; Brauer, M.; Brooks, P.; Bruce, N.G.; Brunekreef, B.; Bryan-Hancock, C.; Bucello, C.; Buchbinder, R.; Bull, F.; Burnett, R.T.; Byers, T.E.; Calabria, B.; Carapetis, J.; Carnahan, E.; Chafe, Z.; Charlson, F.; Chen, H.; Chen, J.S.; Cheng, A.T.; Child, J.C.; Cohen, A.; Colson, K.E.; Cowie, B.C.; Darby, S.; Darling, S.; Davis, A.; Degenhardt, L.; Dentener, F.; Des Jarlais, D.C.; Devries, K.; Dherani, M.; Ding, E.L.; Dorsey, E.R.; Driscoll, T.; Edmond, K.; Ali, S.E.; Engell, R.E.; Erwin, P.J.; Fahimi, S.; Falder, G.; Farzadfar, F.; Ferrari, A.; Finucane, M.M.; Flaxman, S.; Fowkes, F.G.; Freedman, G.; Freeman, M.K.; Gakidou, E.; Ghosh, S.; Giovannucci, E.; Gmel, G.; Graham, K.; Grainger, R.; Grant, B.; Gunnell, D.; Gutierrez, H.R.; Hall, W.; Hoek, H.W.; Hogan, A.; Hosgood, H.D., III; Hoy, D.; Hu, H.; Hubbell, B.J.; Hutchings, S.J.; Ibeanusi, S.E.; Jacklyn, G.L.; Jasrasaria, R.; Jonas, J.B.; Kan, H.; Kanis, J.A.; Kassebaum, N.; Kawakami, N.; Khang, Y.H.; Khatibzadeh, S.; Khoo, J.P.; Kok, C.; Laden, F.; Lalloo, R.; Lan, Q.; Lathlean, T.; Leasher, J.L.; Leigh, J.; Li, Y.; Lin, J.K.; Lipshultz, S.E.; London, S.; Lozano, R.; Lu, Y.; Mak, J.; Malekzadeh, R.; Mallinger, L.; Marcenes, W.; March, L.; Marks, R.; Martin, R.; McGale, P.; McGrath, J.; Mehta, S.; Mensah, G.A.; Merriman, T.R.; Micha, R.; Michaud, C.; Mishra, V.; Mohd Hanafiah, K.; Mokdad, A.A.; Morawska, L.; Mozaffarian, D.; Murphy, T.; Naghavi, M.; Neal, B.; Nelson, P.K.; Nolla, J.M.; Norman, R.; Olives, C.; Omer, S.B.; Orchard, J.; Osborne, R.; Ostro, B.; Page, A.; Pandey, K.D.; Parry, C.D.; Passmore, E.; Patra, J.; Pearce, N.; Pelizzari, P.M.; Petzold, M.; Phillips, M.R.; Pope, D.; Pope, C.A., III; Powles, J.; Rao, M.; Razavi, H.; Rehfuess, E.A.; Rehm, J.T.; Ritz, B.; Rivara, F.P.; Roberts, T.; Robinson, C.; Rodriguez-Portales, J.A.; Romieu, I.; Room, R.; Rosenfeld, L.C.; Roy, A.; Rushton, L.; Salomon, J.A.; Sampson, U.; Sanchez-Riera, L.; Sanman, E.; Sapkota, A.; Seedat, S.; Shi, P.; Shield, K.; Shivakoti, R.; Singh, G.M.; Sleet, D.A.; Smith, E.; Smith, K.R.; Stapelberg, N.J.; Steenland, K.; Stöckl, H.; Stovner, L.J.; Straif, K.; Straney, L.; Thurston, G.D.; Tran, J.H.; Van Dingenen, R.; van Donkelaar, A.; Veerman, J.L.; Vijayakumar, L.; Weintraub, R.; Weissman, M.M.; White, R.A.; Whiteford, H.; Wiersma, S.T.; Wilkinson, J.D.; Williams, H.C.; Williams, W.; Wilson, N.; Woolf, A.D.; Yip, P.; Zielinski, J.M.; Lopez, A.D.; Murray, C.J.; Ezzati, M.; AlMazroa, M.A.; Memish, Z.A. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet, 2012, 380(9859), 2224-2260.
[http://dx.doi.org/10.1016/S0140-6736(12)61766-8] [PMID: 23245609]
[63]
Shih-Ching, K.; Choudhry, M.A.; Matsutani, T.; Schwacha, M.G.; Rue, L.W.; Bland, K.I.; Chaudry, I.H. Splenectomy differentially influences immune responses in various tissue compartments of the body. Cytokine, 2004, 28(3), 101-108.
[http://dx.doi.org/10.1016/j.cyto.2004.07.005] [PMID: 15473952]
[64]
Kleemann, R.; Verschuren, L.; van Erk, M.J.; Nikolsky, Y.; Cnubben, N.H.; Verheij, E.R.; Smilde, A.K.; Hendriks, H.F.; Zadelaar, S.; Smith, G.J.; Kaznacheev, V.; Nikolskaya, T.; Melnikov, A.; Hurt-Camejo, E.; van der Greef, J.; van Ommen, B.; Kooistra, T. Atherosclerosis and liver inflammation induced by increased dietary cholesterol intake: a combined transcriptomics and metabolomics analysis. Genome Biol., 2007, 8(9), R200.
[http://dx.doi.org/10.1186/gb-2007-8-9-r200] [PMID: 17892536]
[65]
Mizukami, T.; Yokoyama, H.; Okamura, Y.; Ohgo, H.; Fukuda, M.; Kamegaya, Y.; Kato, S.; Ishii, H. Splenectomy attenuates superoxide anion release into the hepatic sinusoids after lipopolysaccharide challenge. J. Hepatol., 1999, 31(2), 235-241.
[http://dx.doi.org/10.1016/S0168-8278(99)80219-0] [PMID: 10453935]
[66]
Andriane, Y.; Indriyanti, R.A.; Damailia, R.; Lantika, U.A. Ameliorative effects of ethanol extract of sea cucumber (Holothuria edulis spp.) in alloxan-induced rats. In Medical Technology and Environmental Health: Proceedings of the Medicine and Global Health Research Symposium, Bandung, Indonesia 2020, p. 79.
[67]
Singal, A.K.; Jampana, S.C.; Weinman, S.A. Antioxidants as therapeutic agents for liver disease. Liver Int., 2011, 31(10), 1432-1448.
[http://dx.doi.org/10.1111/j.1478-3231.2011.02604.x] [PMID: 22093324]
[68]
Yu, D.; Chen, G.; Pan, M.; Zhang, J.; He, W.; Liu, Y.; Nian, X.; Sheng, L.; Xu, B. High fat diet-induced oxidative stress blocks hepatocyte nuclear factor 4α and leads to hepatic steatosis in mice. J. Cell. Physiol., 2018, 233(6), 4770-4782.
[http://dx.doi.org/10.1002/jcp.26270] [PMID: 29150932]
[69]
Abu Bakar, M.H.; Azmi, M.N.; Shariff, K.A.; Tan, J.S. Withaferin A protects against high-fat diet-induced obesity via attenuation of oxidative stress, inflammation, and insulin resistance. Appl. Biochem. Biotechnol., 2019, 188(1), 241-259.
[http://dx.doi.org/10.1007/s12010-018-2920-2] [PMID: 30417321]
[70]
Noeman, S.A.; Hamooda, H.E.; Baalash, A.A. Biochemical study of oxidative stress markers in the liver, kidney and heart of high fat diet induced obesity in rats. Diabetol. Metab. Syndr., 2011, 3(1), 17.
[http://dx.doi.org/10.1186/1758-5996-3-17] [PMID: 21812977]
[71]
Odegaard, J.I.; Ricardo-Gonzalez, R.R.; Red Eagle, A.; Vats, D.; Morel, C.R.; Goforth, M.H.; Subramanian, V.; Mukundan, L.; Ferrante, A.W.; Chawla, A. Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell Metab., 2008, 7(6), 496-507.
[http://dx.doi.org/10.1016/j.cmet.2008.04.003] [PMID: 18522831]
[72]
Singh, H.; Bedi, P.S.; Singh, B. Hepatoprotective activity of turmeric and garlic against 7-12, dimethylbenzanthracene induced liver damage in Wistar albino rats. European J. Med. Plants, 2011, 1, 162-170.
[http://dx.doi.org/10.9734/EJMP/2011/587]
[73]
Guo, K.; Su, L.; Wang, Y.; Liu, H.; Lin, J.; Cheng, P.; Yin, X.; Liang, M.; Wang, Q.; Huang, Z. Antioxidant and anti-aging effects of a sea cucumber protein hydrolyzate and bioinformatic characterization of its composing peptides. Food Funct., 2020, 11(6), 5004-5016.
[http://dx.doi.org/10.1039/D0FO00560F] [PMID: 32520032]
[74]
Moghadam, F.D.; Baharara, J.; Balanezhad, S.Z.; Jalali, M.; Amini, E. Effect of Holothuria leucospilota extracted saponin on maturation of mice oocyte and granulosa cells. Res. Pharm. Sci., 2016, 11(2), 130-137.
[PMID: 27168752]
[75]
Soltani, M.; Parivar, K.; Baharara, J.; Kerachian, M.A.; Asili, J. Putative mechanism for apoptosis-inducing properties of crude saponin isolated from sea cucumber (Holothuria leucospilota) as an antioxidant compound. Iran. J. Basic Med. Sci., 2015, 18(2), 180-187.
[PMID: 25810893]
[76]
Kitisin, T.; Suphamungmee, W.; Meemon, K. Saponin-rich extracts from Holothuria leucospilota mediate lifespan extension and stress resistance in Caenorhabditis elegansvia daf-16. J. Food Biochem., 2019, 43(12), e13075.
[http://dx.doi.org/10.1111/jfbc.13075] [PMID: 31612532]

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