Coconut Oil and Cholesterol as Challenge Agents to Induce Hyperlipidemia and Atherosclerosis in Hamster Animal Model
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Vol. 13 No. 1 : 2018 (29-48)
Abstract
Hyperlipidemia is a condition of high lipid levels in the plasma and often linked with the deposition of lipid droplets in the aorta which initiate the progression of atherosclerosis. Atherosclerosis is a common cardiovascular disorder initiated by the formation of foams cells in the vascular wall which leads to turbulent blood flow, injury to the endothelial layer and subsequent vascular thrombosis. Since the early 1980’s, Golden-Syrian hamsters have been widely used as an animal model in the research of hyperlipidemia and atherosclerosis. The use of hamsters in the hyperlipidemic and atherosclerotic model is due to their lipoprotein profile that is closer to human setting, sensitive to high-fat high-cholesterol (HFHC) diet and a suitable rodent model. Atherosclerosis can be induced in hamsters through dietary challenge with HFHC diet. Over the decades, coconut oil (CNO) was commonly used as the source of fat in the diet design of high saturated fatty acids (SFA) composition. In this review, we summarized published literature with designs involving CNO plus cholesterol-induced hyperlipidemia, atherosclerosis or both. The factors that may influence the ability of CNO and cholesterol combination to induce hyperlipidemia such as the period of dietary intervention, hamster strains and the dietary amount were evaluated and summarized.
Keywords :
cardiovascular disease,
diet,
Mesocricetus auratus,
Correspondance Address
Isa Naina-Mohamed. Department of Pharmacology,
Faculty of Medicine, Universiti Kebangsaan Malaysia Medical Centre, Jalan Yaacob Latif, Bandar Tun Razak,
56000 Cheras, Kuala Lumpur, Malaysia. Tel: +603-9145 9568 E-mail: isanaina@ppukm.ukm.edu.my
References
Agbor, G.A., Vinson, J.A., Sortino, J. Johnson,
R. 2012. Antioxidant and anti-atherogenic
activities of three piper species on atherogenic
diet fed hamsters. Exp Toxicol Pathol 64(4):
387-91.
Ahmed, A.A. 2009. Beneficial effects of combined
administration of sodium molybdate with
atorvastatin in hyperlipidemic hamsters. Drug
Discov Ther 3(2): 62-70.
Ahn, Y.S., Smith, D., Osada, J., Li, Z., Schaefer, E.J.
Ordovas, J.M. 1994. Dietary fat saturation
affects apolipoprotein gene expression and high
density lipoprotein size distribution in golden
syrian hamsters. J Nutr 124(11): 2147-55.
Alexaki, A., Wilson, T.A., Atallah, M.T., Handelman,
G. Nicolosi, R.J. 2004. Hamsters fed diets high
in saturated fat have increased cholesterol
accumulation and cytokine production in the
aortic arch compared with cholesterol-fed
hamsters with moderately elevated plasma nonhdl
cholesterol concentrations. J Nutr 134(2):
410-5.
Asami, Y., Yamagishi, I., Akiyoshi, K., Tomoike, H.,
Tsuchida, K. Higuchi, S. 1999. Inhibitory effect of
ts-962 on the formation of early atherosclerotic
lesions in high fat-fed hyperlipidemic hamsters.
Atherosclerosis 146(2): 237-42.
Auger, C., Rouanet, J.M., Vanderlinde, R., Bornet, A.,
Decorde, K., Lequeux, N., Cristol, J.P. Teissedre,
P.L. 2005. Polyphenols-enriched chardonnay
white wine and sparkling pinot noir red wine
identically prevent early atherosclerosis in
hamsters. J Agric Food Chem 53(25): 9823-9.
Ausman, L.M., Rong, N. Nicolosi, R.J. 2005.
Hypocholesterolemic effect of physically
refined rice bran oil: studies of cholesterol
metabolism and early atherosclerosis in
hypercholesterolemic hamsters. J Nutr Biochem
16(9): 521-9.
Bensch, W.R., Gadski, R.A., Bean, J.S., Beavers,
L.S., Schmidt, R.J., Perry, D.N., Murphy, A.T.,
Mcclure, D.B., Eacho, P.I., Breau, A.P., Archer,
R.A. Kauffman, R.F. 1999. Effects of ly295427,
a low-density lipoprotein (LDL) receptor upregulator,
on ldl receptor gene transcription
and cholesterol metabolism in normal and
hypercholesterolemic hamsters. J Pharmacol
Exp Ther 289(1): 85-92.
Bertolotti, M., Spady, D.K. 2001. Inhibition of intestinal
cholesterol absorption by surfomer (alphaolefin
maleic acid) affects hepatic cholesterol
synthesis and low density lipoprotein transport
in hamsters fed a fat-enriched diet. Dig Liver Dis
33(2): 145-50.
Bhatia, G., Rizvi, F., Saxena, R., Puri, A., Khanna,
A.K., Chander, R., Wulff, E.M. Rastogi, A.K.
2003. In vivo model for dyslipidemia with
diabetes mellitus in hamster. Indian J Exp Biol
41(12): 1456-9.
Chen, C.L., Pan, T.M. 2012. Red mold dioscorea: a
potentially safe traditional function food for
the treatment of hyperlipidemia. Food Chem
134(2): 1074-80.
Chen, W., Fan, S., Xie, X., Xue, N., Jin, X. Wang, L.
2014. Novel PPAR pan agonist, ZBH ameliorates
hyperlipidemia and insulin resistance in high fat
diet induced hyperlipidemic hamster. PLoS One
9(4): e96056.
Chen, Y.Y., Lee, P.C., Wu, Y.L. Liu, L.Y. 2015. In vivo
effects of free form astaxanthin powder on
anti-oxidation and lipid metabolism with highcholesterol
diet. PLoS One 10(8): e0134733.
Cherng, J.Y. Shih, M.F. 2005. Preventing dyslipidemia
by chlorella pyrenoidosa in rats and hamsters
after chronic high fat diet treatment. Life Sci
76(26): 3001-13.
Choi, M.S., Jung, U.J., Kim, H.J., Do, G.M., Jeon,
S.M., Kim, M.J. Lee, M.K. 2008. Du-zhong
(Eucommia ulmoides Oliver) leaf extract
mediates hypolipidemic action in hamsters fed
a high-fat diet. Am J Chin Med 36(1): 81-93.
Choi, M.S., Lee, M.K., Jung, U.J., Kim, H.J., Do, G.M.,
Park, Y.B. Jeon, S.M. 2009. Metabolic response
of soy pinitol on lipid-lowering, antioxidant and
hepatoprotective action in hamsters fed-high fat
and high cholesterol diet. Mol Nutr Food Res
53(6): 751-9.
Dalboge, L.S., Pedersen, P.J., Hansen, G., Fabricius,
K., Hansen, H.B., Jelsing, J., Vrang, N. 2015.
A hamster model of diet-induced obesity for
preclinical evaluation of anti-obesity, antidiabetic
and lipid modulating agents. PLoS One
10(8): e0135634.
de Oliveira, F.G., Rossi, C.L., De Oliveira, M.G.,
Saad, M.J. Velloso, L.A. 2000. Effect of
vitamin e supplementation on antibody levels
against malondialdehyde modified ldl in
hyperlipidemic hamsters. Cardiovasc Res 47(3):
567-73.
Delaney, B., Nicolosi, R.J., Wilson, T.A., Carlson, T.,
Frazer, S., Zheng, G.H., Hess, R., Ostergren,
K., Haworth, J. Knutson, N. 2003. Beta-glucan
fractions from barley and oats are similarly
antiatherogenic in hypercholesterolemic syrian
golden hamsters. J Nutr 133(2): 468-75.
Denke, M.A. Grundy, S. 1992. Comparison of effects
of lauric acid and palmitic acid on plasma lipids
and lipoproteins. Am J Clin Nutr 56(5): 895-8.
Dillard, A., Matthan, N.R. Lichtenstein, A.H. 2010.
Use of hamster as a model to study diet-induced
atherosclerosis. Nutr Metab (Lond) 7: 89.
Dillard, A., Matthan, N.R., Spartano, N.L., Butkowski,
A.E. Lichtenstein, A.H. 2013. Background diet
and fat type alters plasma lipoprotein response
but not aortic cholesterol accumulation in f1b
golden syrian hamsters. Lipids 48(12): 1177-84.
Dorfman, S.E., Smith, D.E., Osgood, D.P. Lichtenstein,
A.H. 2003. Study of diet-induced changes
in lipoprotein metabolism in two strains of
Golden-Syrian hamsters. J Nutr 133(12): 4183-8.
Dorfman, S.E., Wang, S., Vega-Lopez, S., Jauhiainen,
M. Lichtenstein, A.H. 2005. Dietary fatty
acids and cholesterol differentially modulate
hdl cholesterol metabolism in golden-syrian
hamsters. J Nutr 135(3): 492-8.
Elson, C.E. 1992. Tropical oils: nutritional and
scientific issues. Crit Rev Food Sci Nutr 31(1-2):
79-102.
Faia, K.L., Davis, W.P., Marone, A.J. Foxall, T.L.
2002. Matrix metalloproteinases and tissue
inhibitors of metalloproteinases in hamster
aortic atherosclerosis: correlation with in-situ
zymography. Atherosclerosis 160(2): 325-37.
Food Drug Administration. 2015. Product
Development under the Animal Rule: Guidance
for Industry. Maryland: FDA.
Foxall, T.L., Shwaery, G.T., Stucchi, A.F., Nicolosi,
R.J. Wong, S.S. 1992. Dose-related effects of
doxazosin on plasma lipids and aortic fatty
streak formation in the hypercholesterolemic
hamster model. Am J Pathol 140(6): 1357-63.
Ghosh, R.K. Ghosh, S.M. 2012. Current status of cetp
inhibitors in the treatment of hyperlipidemia: an
update. Curr Clin Pharmacol 7(2): 102-10.
Ginghina, C., Bejan, I. Ceck, C.D. 2011. Modern risk
stratification in coronary heart disease. J Med
Life 4(4): 377-86.
Goldstein, J.L., Schrott, H.G., Hazzard, W.R.,
Bierman, E.L. Motulsky, A.G. 1973.
Hyperlipidemia in coronary heart disease. Ii.
Genetic analysis of lipid levels in 176 families
and delineation of a new inherited disorder,
combined hyperlipidemia. J Clin Invest 52(7):
1544-68.
Goodnight, S.H., Harris, W.S., Connor, W.E.
Illingworth, D.R. 1982. Polyunsaturated
fatty acids, hyperlipidemia, and thrombosis.
Arteriosclerosis 2(2): 87-113.
Guo, Q., Wang, P.R., Milot, D.P., Ippolito, M.C.,
Hernandez, M., Burton, C.A., Wright, S.D.
Chao, Y.S. 2001. Regulation of lipid metabolism
and gene expression by fenofibrate in hamsters.
Biochim Biophys Acta 1533(3): 220-32.
Hansson, G.K., Robertson, A.K., Söderberg-Nauclér,
C.2006. Inflammation and atherosclerosis.
Annu Rev Pathol 1(1): 297-329.
Hassan, B.A.R. 2013. Overview on Hyperlipidemia. J
Chromat Sep Tech 4(3): e113.
Homburger, F. 1969. Chemical carcinogenesis in the
syrian golden hamster. A review. Cancer 23(2):
313-38.
Huang, T.W., Chang, C.L., Kao, E.S. Lin, J.H. 2015.
Effect of hibiscus sabdariffa extract on high
fat diet-induced obesity and liver damage in
hamsters. Food Nutr Res 59: 29018.
Ioriya, K., Kino, K., Sato, Y.F. Ohashi, N. 2002.
Effect of smp-500, a novel acyl-coa:cholesterol
acyltransferase inhibitor, on serum cholesterol
level and ldl cholesterol clearance in hamsters
with induced hyperlipidemia. Pharmacology
66(2): 107-14.
Jang, E.M., Choi, M.S., Jung, U.J., Kim, M.J., Kim,
H.J., Jeon, S.M., Shin, S.K., Seong, C.N. Lee,
M.K. 2008. Beneficial effects of curcumin on
hyperlipidemia and insulin resistance in highfat-
fed hamsters. Metabolism 57(11): 1576-83.
Jayachandran, M., Chandrasekaran, B.,
Namasivayam, N. 2015. Effect of geraniol,
a plant derived monoterpene on lipids and
lipid metabolizing enzymes in experimental
hyperlipidemic hamsters. Mol Cell Biochem
398(1-2): 39-53.
Jayachandran, M., Chandrasekaran, B. Namasivayam,
N. 2015. Geraniol attenuates oxidative stress by
nrf2 activation in diet-induced experimental
atherosclerosis. J Basic Clin Physiol Pharmacol
26(4): 335-46.
Jorgensen, T., Capewell, S., Prescott, E., Allender,
S., Sans, S., Zdrojewski, T., De Bacquer, D.,
de Sutter, J., Franco, O.H., Logstrup, S., Volpe,
M., Malyutina, S., Marques-Vidal, P., Reiner,
Z., Tell, G.S., Verschuren, W.M. Vanuzzo, D.
2013. Population-level changes to promote
cardiovascular health. Eur J Prev Cardiol 20(3):
409-21.
Kanashiro, A., Kabeya, L.M., Martinello, F., Turato,
W.M., Paula, F.S., Polizello, A.C., Uyemura,
S.A., Lucisano-Valim, Y.M. 2007. Effect of
rutin on polymorphonuclear leukocytes
oxidative metabolism in hypercholesterolemia
golden syrian hamsters: evaluation by
chemiluminescence and flow cytometry.
Pharmazie 62(4): 295-8.
Kim, H.J., Jeon, S.M., Lee, M.K., Cho, Y.Y., Kwon,
E.Y., Lee, J.H. Choi, M.S. 2010. Comparison of
hesperetin and its metabolites for cholesterollowering
and antioxidative efficacy in
hypercholesterolemic hamsters. J Med Food
13(4): 808-14.
Kowala, M.C., Nunnari, J.J., Durham, S.K. Nicolosi,
R.J. 1991. Doxazosin and cholestyramine
similarly decrease fatty streak formation in
the aortic arch of hyperlipidemic hamsters.
Atherosclerosis 91(1-2): 35-49.
Kowala, M.C., Mazzucco, C.E., Hartl, K.S., Seiler,
S.M., Warr, G.A., Abid, S., Grove, R.I.
1993. Prostacyclin agonists reduce early
atherosclerosis in hyperlipidemic hamsters.
Octimibate and bmy 42393 suppress monocyte
chemotaxis, macrophage cholesteryl ester
accumulation, scavenger receptor activity, and
tumor necrosis factor production. Arterioscler
Thromb 13(3): 435-44.
Kowala, M.C., Grove, R.I. Aberg, G. 1994. Inhibitors
of angiotensin converting enzyme decrease
early atherosclerosis in hyperlipidemic
hamsters. Fosinopril reduces plasma cholesterol
and captopril inhibits macrophage-foam cell
accumulation independently of blood pressure
and plasma lipids. Atherosclerosis 108(1): 61-
72.
Kowala, M.C., Recce, R., Beyer, S. Aberg, G.
1995a. Regression of early atherosclerosis in
hyperlipidemic hamsters induced by fosinopril
and captopril. J Cardiovasc Pharmacol 25(2):
179-86.
Kowala, M.C., Rose, P.M., Stein, P.D., Goller, N.,
Recce, R., Beyer, S., Valentine, M., Barton, D.,
Durham, S.K. 1995b. Selective blockade of the
endothelin subtype a receptor decreases early
atherosclerosis in hamsters fed cholesterol. Am
J Pathol 146(4): 819-26.
Krause, B.R., Bousley, R.F., Kieft, K.A., Stanfield,
R.L. 1992. Effect of the acat inhibitor ci-976
on plasma cholesterol concentrations and
distribution in hamsters fed zero- and lowcholesterol
diets. Clin Biochem 25(5): 371-7.
Kumeshini, S., Nurshazana, A., Faizah, O., Kamsiah,
J., Srijit, D., Zar Chi, T. 2016. Development
of hypertensive animal model using
ovariectomised rat fed with short-term 2%
cholesterol diet. Med & Health 11(2): 171-80.
Lecker, J.L., Matthan, N.R., Billheimer, J.T., Rader,
D.J., Lichtenstein, A.H. 2010. Impact of dietary
fat type within the context of altered cholesterol
homeostasis on cholesterol and lipoprotein
metabolism in the F1B hamster. Metabolism
59(10): 1491-501.
Lee, C.L., Hung, Y.P., Hsu, Y.W., Pan, T.M. 2013.
Monascin and ankaflavin have more antiatherosclerosis
effect and less side effect
involving increasing creatinine phosphokinase
activity than monacolin k under the same
dosages. J Agric Food Chem 61(1): 143-50.
Leong, X.F., Ng, C.Y., Jaarin, K. 2015. Animal models
in cardiovascular research: hypertension and
atherosclerosis. Biomed Res Int 2015: 528757.
Lin, Y.L., Chou, C.H., Yang, D.J., Chen, J.W., Tzang,
B.S. Chen, Y.C. 2012. Hypolipidemic and
antioxidative effects of noni (morinda citrifolia l.)
Juice on high- fat/cholesterol-dietary hamsters.
Plant Foods Hum Nutr 67(3): 294-302.
Lin, Y.L., Chang, Y.Y., Yang, D.J., Tzang, B.S. Chen,
Y.C. 2013. Beneficial effects of noni (morinda
citrifolia l.) Juice on livers of high-fat dietary
hamsters. Food Chem 140(1-2): 31-8.
Mangiapane, E.H., Mcateer, M.A., Benson, G.M.,
White, D.A. Salter, A.M. 1999. Modulation of
the regression of atherosclerosis in the hamster
by dietary lipids: comparison of coconut oil and
olive oil. Br J Nutr 82(5): 401-9.
Mawatari, K., Kakui, S., Harada, N., Ohnishi, T., Niwa,
Y., Okada, K., Takahashi, A., Izumi, K. Nakaya,
Y. 2004. Endothelin-1(1–31) levels are increased
in atherosclerotic lesions of the thoracic aorta of
hypercholesterolemic hamsters. Atherosclerosis
175(2): 203-12.
Mcateer, M.A., Grimsditch, D.C., Vidgeon-Hart,
M., Benson, G.M. Salter, A.M. 2007. Dietary
cholesterol reduces lipoprotein lipase activity in
the atherosclerosis-susceptible Bio F1B hamster.
Br J Nutr 89(3): 341-50.
Miedel, E.L. Hankenson, F.C. 2015. Chapter 5 -
Biology and Diseases of Hamsters. In Laboratory
Animal Medicine. 3rd edition. Elsevier Inc.;
209-45.
Mitchell, P.L., Langille, M.A., Currie, D.L. Mcleod,
R.S. 2005. Effect of conjugated linoleic acid
isomers on lipoproteins and atherosclerosis in
the syrian golden hamster. Biochim Biophys
Acta 1734(3): 269-76.
Nelson, R.H. 2013. Hyperlipidemia as a risk factor
for cardiovascular disease. Prim Care 40(1): 195-
211.
Ng, C.H., Qiang Yao, X., Huang, Y. Chen,
Z.Y. 2008. Oxidised cholesterol is more
hypercholesterolaemic and atherogenic than
non-oxidised cholesterol in hamsters. Br J Nutr
99(4): 749-55.
Nicolosi, R.J., Wilson, T.A. Krause, B.R. 1998.
The acat inhibitor, ci-1011 is effective in the
prevention and regression of aortic fatty streak
area in hamsters. Atherosclerosis 137(1): 77-85.
Nirosha, K., Divya, M., Vamsi, S. Sadiq, M. 2014. A
review on hyperlipidemia. Int J Novel Trends
Pharm Sci 4(5): 81-92.
Otto, J., Ordovas, J.M., Smith, D., van Dongen, D.,
Nicolosi, R.J. Schaefer, E.J. 1995. Lovastatin
inhibits diet induced atherosclerosis in f1b
golden syrian hamsters. Atherosclerosis 114(1):
19-28.
Patel, V., Joharapurkar, A., Kshirsagar, S., Patel,
H.M., Pandey, D., Patel, D., Shah, K., Bahekar,
R., Shah, G.B. Jain, M.R. 2017. Central and
peripheral glucagon reduces hyperlipidemia
in rats and hamsters. Drug Res (Stuttg) 67(6):
318-26.
Pereira, P.C., Pernomian, L., Côco, H., Gomes,
M.S., Franco, J.J., Marchi, K.C., Hipólito, U.V.,
Uyemura, S. A., Tirapelli, C.R., de Oliveira, A.M.
2016. Auto-inhibitory regulation of angiotensin
II functionality in hamster aorta during the early
phases of dyslipidemia. Eur J Pharmacol 781:
1-9.
Pitha, J., Bobkova, D., Kovar, J., Havlickova, J.
Poledne, R. 2010. Antiatherogenic effect
of simvastatin is not due to decrease of ldl
cholesterol in ovariectomized golden syrian
hamster. Physiol Res 59(3): 401-6.
Pitman, W.A., Osgood, D.P., Smith, D., Schaefer,
E.J. Ordovas, J.M. 1998. The effects of diet and
lovastatin on regression of fatty streak lesions
and on hepatic and intestinal mrna levels for
the ldl receptor and hmg coa reductase in f1b
hamsters. Atherosclerosis 138(1): 43-52.
Rémillard, P., Shen, G., Milne, R. Maheux, P. 2001.
Induction of cholesteryl ester transfer protein in
adipose tissue and plasma of the fructose-fed
hamster. Life Sci 69(6): 677-87.
Robins, S.J., Fasulo, J.M., Patton, G.M., Schaefer,
E.J., Smith, D.E. Ordovas, J.M. 1995. Gender
differences in the development of hyperlipemia
and atherosclerosis in hybrid hamsters.
Metabolism 44(10): 1326-31.
Rohilla, A., Dagar, N., Rohilla, S., Dahiya, A.,
Kushnoor, A. 2012. Hyperlipidemia- a Deadly
Pathological Condition. Int J Curr Pharm Res
4(2): 15-8. – edi dr google
Romain, C., Bresciani, L., Gaillet, S., Feillet-Coudray,
C., Calani, L., Bonafos, B., Vide, J., Rugani, N.,
Ramos, J., Del Rio, D., Cristol, J.P. Rouanet,
J.M. 2014. Moderate chronic administration
of vineatrol-enriched red wines improves
metabolic, oxidative, and inflammatory markers
in hamsters fed a high-fat diet. Mol Nutr Food
Res 58(6): 1212-25.
Romain, C., Gaillet, S., Carillon, J., Vide, J., Ramos,
J., Izard, J.C., Cristol, J.P. Rouanet, J.M. 2012.
Vineatrol and cardiovascular disease: beneficial
effects of a vine-shoot phenolic extract in a
hamster atherosclerosis model. J Agric Food
Chem 60(44): 11029-36.
Rong, N., Ausman, L.M., Nicolosi, R.J. 1997.
Oryzanol decreases cholesterol absorption and
aortic fatty streaks in hamsters. Lipids 32(3):
303-9.
Russell, J.C. Proctor, S.D. 2006. Small animal models
of cardiovascular disease: tools for the study of
the roles of metabolic syndrome, dyslipidemia,
and atherosclerosis. Cardiovasc Pathol 15(6):
318-30.
Shankar, K., Singh, S.K., Kumar, D., Varshney, S.,
Gupta, A., Rajan, S., Srivastava, A., Beg, M.,
Srivastava, A.K., Kanojiya, S., Mishra, D.K.,
Gaikwad, A.N. 2015. Cucumis melo ssp.
Agrestis var. Agrestis ameliorates high fat diet
induced dyslipidemia in syrian golden hamsters
and inhibits adipogenesis in 3t3-l1 adipocytes.
Pharmacogn Mag 11(Suppl 4): S501-10.
Sima, A., Stancu, C., Constantinescu, E., Ologeanu,
L. Simionescu, M. 2001. The hyperlipemic
hamster-a model for testing the anti-atherogenic
effect of amlodipine. J Cell Mol Med 5(2): 153-
62.
Simionescu, M., Popov, D., Sima, A., Hasu, M.,
Costache, G., Faitar, S., Vulpanovici, A.,
Stancu, C., Stern, D. Simionescu, N. 1996.
Pathobiochemistry of combined diabetes and
atherosclerosis studied on a novel animal
model.The hyperlipemic-hyperglycemic
hamster. Am J Pathol 148(3): 997-1014.
Singh, V., Jain, M., Prakash, P., Misra, A., Khanna, V.,
Tiwari, R.L., Keshari, R.S., Singh, S., Dikshit, M.
Barthwal, M.K. 2011. A time course study on
prothrombotic parameters and their modulation
by anti-platelet drugs in hyperlipidemic
hamsters. J Physiol Biochem 67(2): 205-16.
Singh, V., Jain, M., Misra, A., Khanna, V., Rana,
M., Prakash, P., Malasoni, R., Dwivedi, A.K.,
Dikshit, M. Barthwal, M.K. 2013. Curcuma oil
ameliorates hyperlipidaemia and associated
deleterious effects in golden syrian hamsters. Br
J Nutr 110(3): 437-46.
Singh, V., Rana, M., Jain, M., Singh, N., Naqvi,
A., Malasoni, R., Dwivedi, A.K., Dikshit, M.
Barthwal, M.K. 2015. Curcuma oil attenuates
accelerated atherosclerosis and macrophage
foam-cell formation by modulating genes
involved in plaque stability, lipid homeostasis
and inflammation. Br J Nutr 113(1): 100-13.
Smith, D., Pedro-Botet, J., Cantuti-Castelvetri, I.,
Shukitt-Hale, B., Schaefer, E.J., Joseph, J.
Ordovas, J.M. 2001a. Influence of photoperiod,
laboratory caging and aging on plasma lipid
response to an atherogenic diet among f1b
hamsters. Int J Neurosci 106(3-4): 185-94.
Smith, D., Ahn, Y.S., Pedro-Botet, J., Osada, J., Mata,
P., Schaefer, E.J. Ordovas, J.M. 2001b. Dietary
fat saturation distinctly affects apolipoprotein
gene expression and high density lipoprotein
size distribution in two strains of golden syrian
hamsters. Nutr Res 21(1): 215-28.
Spady, D.K. Dietschy, J.M. 1985. Dietary saturated
triacylglycerols suppress hepatic low density
lipoprotein receptor activity in the hamster.
Proc Natl Acad Sci U S A 82(13): 4526-30.
Srivastava, R.A. 2011. Evaluation of antiatherosclerotic
activities of PPAR-α, PPAR-γ, and
LXR agonists in hyperlipidemic atherosclerosissusceptible
F(1)B hamsters. Atherosclerosis
214(1): 86-93.
Stancu, C.S., Sanda, G.M., Deleanu, M. Sima, A.V.
2014. Probiotics determine hypolipidemic and
antioxidant effects in hyperlipidemic hamsters.
Mol Nutr Food Res 58(3): 559-68.
Stary, H.C., Chandler, A.B., Dinsmore, R.E., Fuster,
V., Glagov, S., Insull, W., Rosenfeld, M.E.,
Schwartz, C. J., Wagner, W.D. Wissler, R.W.
1995. A definition of advanced types of
atherosclerotic lesions and a histological
classification of atherosclerosis. A report from
the committee on vascular lesions of the council
on arteriosclerosis, american heart association.
Circulation 92(5): 1355-74.
Taghibiglou, C., Rudy, D., Van Iderstine, S.C., Aiton,
A., Cavallo, D., Cheung, R. Adeli, K. 2000.
Intracellular mechanisms regulating apobcontaining
lipoprotein assembly and secretion
in primary hamster hepatocytes. J Lipid Res
41(4): 499-513.
Takenaga, T., Imada, K. Otomo, S. 2000.
Hypolipidemic effect of taurine in golden syrian
hamsters. Adv Exp Med Biol 483: 187-92.
Temme, E.H., Mensink, R.P. Hornstra, G. 1996.
Comparison of the effects of diets enriched in
lauric, palmitic, or oleic acids on serum lipids
and lipoproteins in healthy women and men.
Am J Clin Nutr 63(6): 897-903.
Townsend, N., Nichols, M., Scarborough, P. Rayner,
M. 2015. Cardiovascular disease in europeepidemiological
update 2015. Eur Heart J
36(40): 2696-705.
Trautwein, E.A., Jingsheng, L. Hayes, K.C. 1993.
Plasma lipoproteins, biliary lipids and bile acid
profile differ in various strains of syrian hamsters
Mesocricetus auratus. Comp Biochem Physiol
Comp Physiol 104(4): 829-35.
Tsutsumi, K., Hagi, A. Inoue, Y. 2001. The
relationship between plasma high density
lipoprotein cholesterol levels and cholesteryl
ester transfer protein activity in six species of
healthy experimental animals. Biol Pharm Bull
24(5): 579-81.
Uehara, Y., Urata, H., Ideishi, M., Arakawa, K. Saku,
K. 2002. Chymase inhibition suppresses highcholesterol
diet-induced lipid accumulation in
the hamster aorta. Cardiovasc Res 55(4): 870-6.
Vide, J., Virsolvy, A., Romain, C., Ramos, J., Jouy,
N., Richard, S., Cristol, J.P., Gaillet, S. Rouanet,
J.M. 2015. Dietary silicon-enriched spirulina
improves early atherosclerosis markers in
hamsters on a high-fat diet. Nutrition 31(9):
1148-54.
Vinson, J.A., Mandarano, M.A., Shuta, D.L., Bagchi,
M. Bagchi, D. 2002. Beneficial effects of a novel
ih636 grape seed proanthocyanidin extract
and a niacin-bound chromium in a hamster
atherosclerosis model. Mol Cell Biochem
240(1-2): 99-103.
Vinson, J.A., Teufel, K. Wu, N. 2001. Red wine,
dealcoholized red wine, and especially grape
juice, inhibit atherosclerosis in a hamster
model. Atherosclerosis 156(1): 67-72.
Wang, X., Guan, L., Zhao, Y., Lei, L., Liu, Y., Ma,
K.Y., Wang, L., Man, S.W., Wang, J., Huang, Y.
Chen, Z.Y. 2015. Plasma cholesterol-lowering
activity of dietary dihydrocholesterol in
hypercholesterolemia hamsters. Atherosclerosis
242(1): 77-86.
Wang, Z., Niimi, M., Ding, Q., Liu, Z., Wang, L.,
Zhang, J., Xu, J. Fan, J. 2017. Comparative studies
of three cholesteryl ester transfer proteins and
their interactions with known inhibitors. PLoS
One 12(8): e0180772.
Warner, B.M., Safronetz, D. Kobinger, G.P. 2017.
Syrian hamsters as a small animal model for
emerging infectious diseases: advances in
immunologic methods. Adv Exp Med Biol 972:
87-101.
Weingand, K.W. Daggy, B.P. 1991. Effects of dietary
cholesterol and fasting on hamster plasma
lipoprotein lipids. Eur J Clin Chem Clin Biochem
29(7): 425-8.
Wilkins, E., Wilson, L., Wickramasinghe, K.,
Bhatnagar, P., Leal, J., Luengo-Fernandez, R.,
Burns, R., Rayner, M., Townsend, N. 2017.
European Cardiovascular Disease Statistics
2017. European Heart Network: Brussels.
Wilson, T.A., Meservey, C.M. Nicolosi, R.J. 1998a.
Soy lecithin reduces plasma lipoprotein
cholesterol and early atherogenesis in
hypercholesterolemic monkeys and hamsters:
beyond linoleate. Atherosclerosis 140(1): 147-
53.
Wilson, T.A., Romano, C., Liang, J. Nicolosi,
R.J. 1998b. The hypocholesterolemic and
antiatherogenic effects of cholazol h, a
chemically functionalized insoluble fiber with
bile acid sequestrant properties in hamsters.
Metabolism 47(8): 959-64.
Wilson, T.A., Nicolosi, R.J., Lawton, C.W. Babiak,
J. 1999. Gender differences in response to
a hypercholesterolemic diet in hamsters:
effects on plasma lipoprotein cholesterol
concentrations and early aortic atherosclerosis.
Atherosclerosis 146(1): 83-91.
Wilson, T.A., Foxall, T.L. Nicolosi, R.J. 2003.
Doxazosin, an alpha-1 antagonist, prevents
further progression of the advanced
atherosclerotic lesion in hypercholesterolemic
hamsters.Metabolism 52(10): 1240-5.
Wilson, T.A., Nicolosi, R.J., Kotyla, T., Sundram,
K. Kritchevsky, D. 2005. Different palm oil
preparations reduce plasma cholesterol
concentrations and aortic cholesterol
accumulation compared to coconut oil in
hypercholesterolemic hamsters. J Nutr Biochem
16(10): 633-40.
Wilson, T.A., Nicolosi, R.J., Saati, A., Kotyla, T.
Kritchevsky, D. 2006a. Conjugated linoleic
acid isomers reduce blood cholesterol levels
but not aortic cholesterol accumulation in
hypercholesterolemic hamsters. Lipids 41(1):
41-8.
Wilson, T.A., Kritchevsky, D., Kotyla, T. Nicolosi,
R.J. 2006b. Structured triglycerides containing
caprylic (8:0) and oleic (18:1) fatty acids reduce
blood cholesterol concentrations and aortic
cholesterol accumulation in hamsters. Biochim
Biophys Acta 1761(3): 345-9.
Wilson, T.A., Nicolosi, R.J., Woolfrey, B. Kritchevsky,
D. 2007. Rice bran oil and oryzanol reduce
plasma lipid and lipoprotein cholesterol
concentrations and aortic cholesterol ester
accumulation to a greater extent than ferulic
acid in hypercholesterolemic hamsters. J Nutr
Biochem 18(2): 105-12.
Zha, W., A, J., Wang, G., Yan, B., Gu, S., Zhu, X.,
Hao, H., Huang, Q., Sun, J., Zhang, Y., Cao, B.
Ren, H. 2009. Metabonomic characterization of
early atherosclerosis in hamsters with induced
cholesterol. Biomarkers 14(6): 372-80.
Zhao, M.J., Wang, S.S., Jiang, Y., Wang, Y., Shen, H.,
Xu, P., Xiang, H. Xiao, H. 2017. Hypolipidemic
Effect of Xh601 on Hamsters of Hyperlipidemia
and Its Potential Mechanism. Lipids Health Dis
16(1): 85.
Zhao, Y., Shu, P., Zhang, Y., Lin, L., Zhou, H., Xu, Z.,
Suo, D., Xie, A. Jin, X. 2014. Effect of centella
asiatica on oxidative stress and lipid metabolism
in hyperlipidemic animal models. Oxid Med
Cell Longev 2014: 7.
