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Effect of long-term optional ingestion of canola oil, grape seed oil, corn oil and yogurt butter on serum, muscle and liver cholesterol status in rats
Food and Chemical Toxicology 48 (2010) 2454–2457
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Effect of long-term optional ingestion of canola oil, grape seed oil, corn oil and yogurt butter on serum, muscle and liver cholesterol status in rats Farzad Asadi a,*, Ali Shahriari b, Marjan Chahardah-Cheric b a b
Department of Biochemistry, School of Veterinary Medicine, University of Tehran, Azadi Street, Tehran, Iran Department of Biochemistry, School of Veterinary Medicine, Shahid Chamran University, Ahvaz, Iran
a r t i c l e
i n f o
Article history: Received 5 April 2010 Accepted 7 June 2010
Keywords: Canola oil Grape seed oil Corn oil Yogurt butter Cholesterol Rat
a b s t r a c t The aim of the present study was to determine the effect of long-term optional intake of vegetable oils (canola, grape seed, corn) and yogurt butter on the serum, liver and muscle cholesterol status. Twenty-five male Wistar rats were randomly categorized into five groups (n = 5) as follows: control, canola oil, grape seed oil, corn oil and manually prepared yogurt butter. In each group, 24 h two bottle choice (oil and water) tests were performed for 10 weeks. Serum cholesterol values showed a trend to decrease in grape seed oil, corn oil and yogurt butter groups compared to the control. Optional intake of yogurt butter made a significant increase in HDL-C values (42.34 ± 9.98 mg/dL) yet decrease in LDLC values (11.68 ± 2.06 mg/dL) compared to the corresponding control (19.07 ± 3.51; 30.96 ± 6.38 mg/dL, respectively). Furthermore, such findings were concomitant with a significant decrease in the liver TC levels (1.75 ± 0.31 mg/g liver) and an increase in the muscle TC levels (1.85 ± 0.32 mg/g liver) compared to the corresponding control (2.43 ± 0.31; 0.94 ± 0.14 mg/g liver, respectively). Optional intake of manually prepared yogurt butter has more beneficial effects on serum lipoprotein cholesterol values with some alterations in the liver and muscle cholesterol states than the vegetable oils. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction A source of cholesterol for high density lipoprotein cholesterol (HDL-C) is derived from cellular cholesterol. The effect of changing the quality of dietary fat on cholesterol synthesis is controversial. While several studies have indicated that whole body cholesterol synthesis is unchanged (Valsta et al., 1992; Markelova et al., 1970) others have documented decreased or increased rates when polyunsaturated fatty acids replace saturated fatty acids in the diet (Coiffier et al., 1987; Wardlaw et al., 1991). Moreover, these studies indicate that serum cholesterol levels are raised with consumption of fats containing saturated fatty acids and reduced with fats rich in polyunsaturated fatty acids. There are some controversies about the effects of oil and fat consumptions in the human societies. The fat derived from dairy products is one of the most widely consumed fats in the human population. There are some controversies about the effect of milk fat on the health status and serum lipid and lipoprotein parameters in human population. In this respect, some investigators showed a reverse association between milk fat consumption and risk of coronary artery diseases (Seidel et al., 2005; Elwood et al., 2004). However, some studies showed a reduction in the plasma risk fac-
* Corresponding author. Tel.: +98 2161117130; fax: +98 2166933222. E-mail address: [email protected] (F. Asadi). 0278-6915/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.fct.2010.06.012
tors of the atherosclerotic diseases due to milk fat consumption (Sjogren et al., 2004; Tricon et al., 2006). We have previously shown that long-term ingestion of corn oil rich diet can make deleterious effects on serum cholesterol levels (Asadi et al., 2008). Meanwhile, Takeda et al. (2000) and Imaizumi et al. (2001) investigated the effect of long-term optional ingestion of corn oil on the caloric intake and obesity in mice (Takeda et al., 2000; Imaizumi et al., 2000). They showed that mice continued to prefer corn oil and consequently developed excessive caloric intake and obesity (Takeda et al., 2001). Investigators believe that relationship between dietary fat saturation and cholesterol metabolism is a complex matter in relation to type of dietary fat, their fatty acid composition and the level of intake (Luzfernandez et al., 1996). On the other hand, differential oil intakes of rats have been documented among high fat diet and high carbohydrate diet so that high fat diet increased their intake and preference for oil (Reed et al., 1990). Meanwhile, high fat foods such as those sold in cafeterias and supermarkets are often preferred by most people. Intake of high palatable oily or fatty foods often induces excessive caloric consumption and obesity (Takeda et al., 2001). Reports linking dietary fat to serum lipid levels have been interpreted as meaning that the general public, especially those at risk of coronary heart disease, should consume low fat diets. They argued that dietary saturated fatty acids elevated serum cholesterol concentrations, whereas polyunsaturated fatty acids reduced serum cholesterol
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concentrations and mono-unsaturated have little or no effect (KrisEtherton and Fosmire, 1984; Beynen et al., 1987a; Mattson and Grundy, 1985). Changes in the cellular cholesterol status and HDL-C values in response to different parameters have been discussed by some investigators. In this regard, the enhancing effect of exercise on HDL-C concentration has been documented (Durstine et al., 2001). In this respect, Sviridov et al., (2003) showed that additional sources of HDL-C might be derived from exercising muscle as other lipids are utilized for fuel (Sviridov et al., 2003). Moreover, it is possible that when cells become depleted of triglyceride, cellular cholesterol is also mobilized and released to its primary acceptor, HDL (Sviridov et al., 2003). Kiens and Lithell (1989) attributed post exercise increase in HDL-C concentrations to degradation of VLDL. Interestingly, Ruys et al. (1989) showed an increase in HDL production in the exercising forearm of individual who had eaten a fat meal. It has been shown that oils will be preferentially ingested by rats according to their flavors (Takeda et al., 2000; Ackroff et al., 1990). Therefore, the aim of this preliminary study was to compare the contribution of long-term optional ingestion of different vegetable oils (canola, grape seed and corn) and yogurt butter on the serum cholesterol status and the cholesterol levels in the liver and muscle in rats.
2. Materials and methods Twenty-five Wistar rats (224.83 ± 31.93 g) were purchased from the Pasteur Institute (Tehran, Iran). All rats were acclimatized in the animal house (12-h light: 12-h dark at 22 ± 2 °C) for 10 days and received a regular chow diet. Diets were purchased from Dam Pars Company (Tehran, Iran). After the acclimation period rats were randomly categorized to five groups of five rats each. Each group was maintained in a separate cage. Each cage was equipped with two bottles of water and oil except the control group (only water). Treatment groups of canola oil, grape seed oil, corn oil and yogurt butter optionally drank 100% of canola oil, grape seed oil, corn oil and yogurt butter for 10 weeks, respectively. Canola oil (C16:0, 4%; C18:0, 2%; C18:1, 62%; C18:2, 22%; C18:3, 10%), corn oil (C16:0, 11%; C18:0, 2%; C18:1, 28%; C18:2, 58%; C18:3, 1%) and grape seed oil (C16:0, 8%; C18:0, 4%; C18:1, 15%; C18:2, 73%) were purchased as commercial grade. Cow’s yogurt butter was prepared from previous day’s yogurt. Cows were reared in southwestern Iran (Bagh Malek, Khozestan, Iran). In this regard, cow’s milk yogurt from the previous day’s yogurt was churned for about 1 h, butter fat collected and gently heated to melt and formed into butter. In turn we centrifuged it for collecting the pure butter. Yogurt butter prepared, aliquoted and freezed at 80 °C until use. All procedures involving animals were approved by the Animal Care Association of the Department of Basic Sciences, School of Veterinary Medicine, University of Tehran (Tehran, Iran). Fatty acid profiles of Yogurt butter were determined by using a gas chromatograph (Agilent 6890, Oilseed Research and Development Company, Tehran, Iran) equipped with a BPX-&) column (12 m, 25 lm i.d., 0.2 lm film thickness). The column temperature was held at 45 °C for 4 min, increased to 175 °C at a rate of 13 °C/ min, to 215 °C at 4 °C and held for 60 min. Fatty acid methyl esters were identified on the basis of ISO 5508 (ISIRI 4090) and analyzed according to the ISO 5509 (ISIRI 4091). At the end of 10 weeks, rats were exsanguinated through cardiac puncture after a 12-h fast (water ad libitum). Serum concentrations of total cholesterol (TC) were measured using the cholesterol oxidase p-aminophenazone method. High density lipoprotein cholesterol (HDL-C) concentrations were measured by precipitation of apoB-containing lipoprotein with manganese-heparin and measurement of cholesterol in the supernatant according to the method of Burstein et al. (1970) with reagents prepared by Research Company (Anzan Chimie Mandegar Company, Tehran, Iran). Low density lipoprotein cholesterol (LDL-C) concentrations were measured using prepared reagents according to manufacturer instruction and calibrated with the calibrator provided by the manufacturer (Pars Azmun Company, Tehran, Iran). The livers were extracted and lipid extraction was done according to the Hara and Radin (1978) method. Briefly, in a test tube, 0.5 g of liver tissue was weighed and 9 mL of hexane:isopropanol (3:2) was added. Glass beads (2.5 mm diameter) were then added to each tube and shaken overnight. This mixture was then centrifuged at 1000g for 15 min and the supernatant was removed, mixed with 12 mL of aqueous Natrium sulfate (6.6%) and decanted for 15 min. The supernatant was then removed, dried and reconstituted in 1.5 mL of isopropanol for lipid analysis. TC of liver was estimated by the enzymatic method for each animal. Leg muscle samples were chopped and minced with mortar and pestle. An aliquot (1 g) of the sample was taken for lipid extraction and TC measured for each animal as mentioned for liver, previously.
The arrangement of data and the calculation of the mean and SD for each value was done in Microsoft Excel 2007. For each parameter, statistical analysis were done by one way ANOVA among groups using Sigma Stat 2.0 (Systat Software Inc., Point Richmond, CA). Alpha in all cases was 5% (p < 0.05).
3. Results Yogurt fatty acid profiles are tabulated in Table 1. Saturated fatty acids C16:0, C14:0 and C18:0 constitute the major fatty acids of yogurt butter. Table 2 shows oil and feed intake of rats. Rats showed a significant preference for vegetable oil intake compared to yogurt butter (p < 0.001). However, there was not any difference among vegetable oils. On the other hand, all treatment groups showed significant decrease in feed intake when compared to the control (p < 0.001). Serum TC, HDL-C and LDL-C concentrations are tabulated in Table 2. While canola oil and corn oil made decreased (about 36% and 21%, respectively) serum TC levels, significant changes were not shown in other groups when compared to the control. However, we have shown a trend to decrease in serum TC levels in all groups when compared to the control. Interestingly, while vegetable oils had any effect on the serum HDL-C concentrations, yogurt butter made a significant increase (about 122%) in serum HDL-C concentrations compared to the control (p < 0.001). Furthermore, yogurt butter decreased LDL-C concentrations (about 62%), conversely. On the other hand, a decrease in LDL-C values (about 64%) was shown for canola oil. While the amount of feed yogurt butter is not comparable with the amount of feed vegetable oils, optional intake of yogurt butter made a significant increase in the muscle TC levels (p < 0.001) and decreased liver TC levels when compared to the control (p = 0.026). In this respect, vegetable oils had no effect on the muscle and liver TC levels, except grape seed oil which decreased liver TC as much as yogurt butter. In spite of these changes, BMI scores showed the same status in all treatment groups. 4. Discussion In the present study, rats were given vegetable oils and yogurt butter solution as an optional supplement to their regular chow. Rats showed preference for optional ingestion of vegetable oils than yogurt butter. However, optional ingestion of these oils and fat made a significant decrease in feed intake. Takeda et al. (2001) argued that this condition is due to excess caloric intake in rats. Interestingly, we have shown that this increase in caloric intake is concomitant with an increase in the muscle TC and serum HDL-C values and a decrease in liver TC and LDL-C values due to
Table 1 Fatty acid composition of yogurt butter. S-SCFA (%)
S-MCFA (%)
S-LCFA (%)
Un-saturated FA (%)
C4 (2.70) C6 (2.53) C8 (1.79) C10 (4.13) C12(4.85)
C14 (14.98) C15 (1.69) C16 (38.88) C17(0.80)
C18 C20 C22 C21 C24
C10:1 C14:1 C16:1 C17:1 C18:1 C18:1 C18:2 C18:2 C20:1 C20:2 C21:1
(11.72) (0.65) (0.23) (0.10) (0.04)
(0.47) (2.29) (3.58) (0.36) trans (2.06) Cis (2.06) trans (0.34) Cis (3.36) (0.19) (0.09) (0.10)
Values were expressed as percent by weights. SCFA, saturated-short chain fatty acid; S-MCFA, saturated medium chain fatty acid; S-LCFA, saturated long chain fatty acid.
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Table 2 Serum cholesterol (TC), high density lipoprotein cholesterol (HDL-C), low density lipoprotein cholesterol (LDL-C), body mass index (BMI), liver TC, muscle TC, feed intake and oil and fat intake after 10 weeks of optional intake of different vegetable oils (canola, grape seed, corn) and yogurt butter in the corresponding rat groups (n = 5). Values were expressed as mean ± SD. Values of each parameter compared among groups using one-way ANOVA. Group
TC (mg/dl)
HDL-C (mg/dl)
LDL-C (mg/dl)
Liver TC (mg/g liver)
Muscle TC (mg/g liver)
10 Weeks Feed intake (g)
10 Weeks oil and butter intake (g)
BMI (kg/m2)
Control (I) Canola oil (II) Grape seed oil (III) Corn oil (IV) Yogurt butter (V) p-Values (differences among groups)
70.19 ± 9.64 45.03 ± 6.79 59.60 ± 10.44 55.81 ± 6.51 64.23 ± 9.74 I, II (<0.001); I, IV(0.017); II, V(0.002); II, III(0.016);
19.07 ± 3.51 16.75 ± 2.70 14.59 ± 2.49 18.26 ± 3.24 42.34 ± 9.98 I, V; II, V; III, V; IV, V (<0.001)
30.96 ± 6.38 11.28 ± 1.75 28.06 ± 6.41 22.86 ± 6.10 11.68 ± 2.06 I,II (<0.001); I, V(<0.001); I, IV(0.019); II, III(<0.001); III, (<0.001); II, IV(<0.00); IV, V(<0.001)
2.43 ± 0.31 2.74 ± 0.41 1.77 ± 0.74 2.50 ± 0.42 1.75 ± 0.31 I, III(0.037); I, V(0.032); II, V(0.003); II, III(0.004); IV, V(0.019); III, IV(0.022)
0.94 ± 0.14 0.93 ± 0.07 0.91 ± 0.15 0.91 ± 0.11 1.85 ± 0.32 I, V; II, V; III, V; IV, V (<0.001)
115.61 ± 18.32 87.15 ± 12.18 89.61 ± 12.49 90.63 ± 17.81 94.52 ± 11.82 I, II(0.006); I, III(0.012); I, IV(0.015); I, V(<0.001)
0 6.84 ± 1.93 7.34 ± 2.31 7.11 ± 1.61 1.91 ± 0.74 II, IV; III, V; IV, V (<0.001)
5.74 ± 0.51 5.74 ± 0.33 5.73 ± 0.73 5.97 ± 0.78 5.92 ± 0.42 No
the optional ingestion of yogurt butter. This beneficial effect of yogurt butter may be due to applied yogurt butter production process. In the present study we used a manually produced unpurified butter. It seems that this procedure is less harmful for useful compounds of yogurt butter compared to the manufacturing procedure. In line with our findings, Tholstrup et al. (2004) declared that some hypocholesterolemic factors associated with some milk products may be removed during the butter production process. Furthermore, the effect of regular intake of milk fat on the lipid and lipoprotein metabolism has been discussed by Haug et al. (2008). They argued that the moderate intake of milk fat may reduce the risk of atherosclerotic diseases due to a reduction in small dense low density lipoprotein particles. This property of the milk fat can be attributed to its conjugated linoleic acid ingredients (Haug et al., 2008). Hence, this can be deduced that milk contains a beneficial milk factor which somehow modulates the cholesterol raising effect of the milk fat. As can be seen in Table 1, saturated and mono-unsaturated fatty acids constitute the major components of yogurt butter. Therefore, these favorable effects cannot be attributed to its polyunsaturated fatty acids as is right in vegetable oils. This hypothesis is in line with a finding that whole milk reduces plasma and hepatic TG in rats. This condition has been discussed with some investigators so that they believe a high intake of whole milk is associated with a low risk of coronary artery disease in middle-aged men in a manner that cannot simply be predicted by the fat content of whole milk (Tholstrup et al., 1998). Moreover, similar status has been argued in physically active people who received dairy products by Sviridov et al. (2003). However, these investigators did not mention the required amount of exercise or dairy products on its protective effect. Our findings about the optional intake of diet supplemented with manually prepared milk fat may be a novel finding in this regard. They believe that these effects of dietary fat on cholesterol status could potentially be attributable to factors including fatty acid consumption or the presence of plant sterols or other constituents. Can these factors have an effects on the muscle TC levels? Moreover, is it possible for muscle TC to contribute in HDL-C synthesis due to the optional intake of these unpurified fat? Or is this condition is due to their effects on the hepatic pre-b HDL synthesis? All of these questions should be investigated in future studies. Chung et al. (2003) studied the effect of isoflavone and/or grape seed oil supplementation on blood lipid profiles and bone strength in ovariectomised female rats. In the present study, we have shown a significant decrease in liver TC levels due to the intake of grape seed oil and milk fat. Chung et al. (2003) found that after 8 weeks feeding of grape seed oil supplementation to rats it decreased TC, TG and LDL-C levels, yet crude lipid and TC contents in liver were
not affected in this condition. In this regard, it has been previously shown that diets rich in either olive or canola oils appeared to increase serum HDL-C concentrations. Moreover, reducing total fat calories in the diet decreased both plasma LDL-C and HDL-C concentrations (Mattson and Grundy, 1985). It has been documented that the intake of mono-unsaturated fatty acids compared with polyunsaturated fatty acids will be resulted in increased plasma cholesterol levels in rats (Kris-Etherton and Fosmire, 1984; Beynen et al., 1987b). Analysis of the canola, grape seed and corn oils showed that they are rich in mono-unsaturated fatty acid (oleic acid), linoleic acid and n-6 polyunsaturated fatty acid, respectively. Karvonen et al. (2002) showed the effect of rape seed oil based cheese (milk fat substituted by rape seed oil) on serum TC and lipoprotein lipid concentrations in reference to ordinary milk fat based cheese in subjects with mildly to moderately elevated serum cholesterol concentration. They showed that rape seed oil based cheese reduced serum TC and LDL-C concentrations in mildly to moderately hypercholesterolemic subjects when replacing ordinary milk fat based cheese in the diet. In present study, we have shown a trend to decrease in serum TC levels and a significant decrease in the levels of LDL-C in canola oil, corn oil and yogurt butter groups. However, we have not been able to show the beneficial effects of grape seed oil on HDL-C and LDL-C values when used as optional ingestion. It seems that optional grape seed oil ingestion makes its effect by changing cellular (muscle and liver) cholesterol status than the serum cholesterol parameters. Some disagreements in the findings show that the regular intake of grape seed oil has beneficial effects on serum HDL-C in human subjects. In this an respect increase in serum HDL-C levels and a decrease in LDL-C levels, TC/HDL-C and LDL-C/HDL-C ratios have been reported. They have shown that up to 45 g intake of grape seed oil per day raised HDL-C levels by 13%, reduced LDL-C levels by 7%, decreased TC/HDL-C ratio by 15.6% and reduced LDL-C/HDL-C ratio by 15.3% in 3 weeks (Uma Maheswari and Rao, 2005; Nash, 2004). The present report revealed that optional supplement of canola oil to the normal diet reduced serum TC concentrations with respect to the control. Such a status can be attributed to its high level of polyunsaturated fatty acids in combination with mono-unsaturated fatty acids.
5. Conclusion It seems yogurt butter has some beneficial factors for changing serum and liver cholesterol status. These preliminary findings would be investigated in future for checking the effect of different
F. Asadi et al. / Food and Chemical Toxicology 48 (2010) 2454–2457
yogurt butter production procedures on the probable beneficial factors which may work in a single or cooperative manner. Furthermore, it seems that the optional ingestion of canola and corn oils have beneficial effects on the serum cholesterol status and grape seed oil on the liver cholesterol values without adverse effects on HDL-C and BMI status. Such effects probably make these oils safe additives for use. Conflict of Interest The authors declare that there are no conflicts of interest. References Ackroff, K., Vigorito, M., Sclafani, A., 1990. Fat appetite in rats: The response of infant and adult rats to nutritive and non-nutritive oil emulsions. Appetite 15, 171– 188. Asadi, F., Shahriari, A., Pourkabir, M., Maclaren, R., 2008. Short and long-term effect of corn oil on serum lipid and lipoprotein and visceral abdominal fat pad parameters of rats. Journal of Food Lipids 15, 68–80. Beynen, A.C., Versluis, A., Katan, M.B., Van Zutphen, L.F.M., 1987a. Interaction of dietary cholesterol with the type of fat and fiber with regard to plasma cholesterol response in rabbits. Nutrition Reports International 35, 355–360. Beynen, A.C., Visser, J.J., Schouten, J.A., Katan, M.B., 1987b. Cholesterol metabolism in rabbits fed diets containing either corn oil or olive oil. Nutrition Reports International 35, 111–116. Burstein, M., Scholnick, H.R., Morfin, R., 1970. Rapid method for the isolation of lipoprotein from human serum by precipitation with polyanions. Journal of Lipid Research 11, 583–595. Chung, H.K., Choes, C.S., Lee, J.H., Park, W.J., Kang, M.H., 2003. The effect of isoflavone and/or grape seed oil supplementation on blood lipid profiles and bone strength in ovariectomized female rats. Korean Journal of Nutrition 36, 667–674. Coiffier, E., Paris, R., Lecer, F.J., 1987. Effects of dietary saturated and polyunsaturated fat on lipoprotein and hepatic triglyceride lipase activity. Comparative Biochemistry and Physiology – Part B: Biochemistry & Molecular Biology 88, 187–192. Durstine, J.L., Grandjean, P.W., Davis, P.G., Ferguson, M.A., Alderson, N.L., DuBose, K.D., 2001. Blood lipid and lipoprotein adaptation to exercise: A quantitative analysis. Sports Medicine 31, 1033–1062. Elwood, P.C., Pickering, J.E., Hughes, J., Fehily, A.M., Ness, A.R., 2004. Milk drinking, ischaemic heart disease and ischaemic stroke. II. Evidence from cohort studies. European Journal of Clinical Nutrition 58, 18–724. Hara, A., Radin, N.S., 1978. Lipid extraction of tissue with a low toxicity solvent. Analytical Biochemistry 90, 420–426. Haug, A., Sjogren, P., Holland, N., Muller, H., Kjos, N., Taugbol, O., Fjerdingby, N., Biong, A.S., Selmer-Olsen, E., Harstad, O.M., 2008. Effects of butter naturally enriched with conjugated linoleic acid and vaccenic acid on blood lipids and LDL particle size in growing pigs. Lipids in Health and Disease 731. doi:10.1186/ 1476-S11x-7-31. Imaizumi, M., Takeda, M., Fushiki, T., 2000. Effects of oil intake in the conditioned place preference test in mice. Brain Research 870, 150–156. Imaizumi, M., Takeda, M., Sawano, S., Fushiki, T., 2001. Opioidergic contribution to conditioned place preference induced by corn oil in mice. Behavioural Brain Research 121, 129–136.
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Food and Chemical Toxicology journal homepage: www.elsevier.com/locate/foodchemtox
Effect of long-term optional ingestion of canola oil, grape seed oil, corn oil and yogurt butter on serum, muscle and liver cholesterol status in rats Farzad Asadi a,*, Ali Shahriari b, Marjan Chahardah-Cheric b a b
Department of Biochemistry, School of Veterinary Medicine, University of Tehran, Azadi Street, Tehran, Iran Department of Biochemistry, School of Veterinary Medicine, Shahid Chamran University, Ahvaz, Iran
a r t i c l e
i n f o
Article history: Received 5 April 2010 Accepted 7 June 2010
Keywords: Canola oil Grape seed oil Corn oil Yogurt butter Cholesterol Rat
a b s t r a c t The aim of the present study was to determine the effect of long-term optional intake of vegetable oils (canola, grape seed, corn) and yogurt butter on the serum, liver and muscle cholesterol status. Twenty-five male Wistar rats were randomly categorized into five groups (n = 5) as follows: control, canola oil, grape seed oil, corn oil and manually prepared yogurt butter. In each group, 24 h two bottle choice (oil and water) tests were performed for 10 weeks. Serum cholesterol values showed a trend to decrease in grape seed oil, corn oil and yogurt butter groups compared to the control. Optional intake of yogurt butter made a significant increase in HDL-C values (42.34 ± 9.98 mg/dL) yet decrease in LDLC values (11.68 ± 2.06 mg/dL) compared to the corresponding control (19.07 ± 3.51; 30.96 ± 6.38 mg/dL, respectively). Furthermore, such findings were concomitant with a significant decrease in the liver TC levels (1.75 ± 0.31 mg/g liver) and an increase in the muscle TC levels (1.85 ± 0.32 mg/g liver) compared to the corresponding control (2.43 ± 0.31; 0.94 ± 0.14 mg/g liver, respectively). Optional intake of manually prepared yogurt butter has more beneficial effects on serum lipoprotein cholesterol values with some alterations in the liver and muscle cholesterol states than the vegetable oils. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction A source of cholesterol for high density lipoprotein cholesterol (HDL-C) is derived from cellular cholesterol. The effect of changing the quality of dietary fat on cholesterol synthesis is controversial. While several studies have indicated that whole body cholesterol synthesis is unchanged (Valsta et al., 1992; Markelova et al., 1970) others have documented decreased or increased rates when polyunsaturated fatty acids replace saturated fatty acids in the diet (Coiffier et al., 1987; Wardlaw et al., 1991). Moreover, these studies indicate that serum cholesterol levels are raised with consumption of fats containing saturated fatty acids and reduced with fats rich in polyunsaturated fatty acids. There are some controversies about the effects of oil and fat consumptions in the human societies. The fat derived from dairy products is one of the most widely consumed fats in the human population. There are some controversies about the effect of milk fat on the health status and serum lipid and lipoprotein parameters in human population. In this respect, some investigators showed a reverse association between milk fat consumption and risk of coronary artery diseases (Seidel et al., 2005; Elwood et al., 2004). However, some studies showed a reduction in the plasma risk fac-
* Corresponding author. Tel.: +98 2161117130; fax: +98 2166933222. E-mail address: [email protected] (F. Asadi). 0278-6915/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.fct.2010.06.012
tors of the atherosclerotic diseases due to milk fat consumption (Sjogren et al., 2004; Tricon et al., 2006). We have previously shown that long-term ingestion of corn oil rich diet can make deleterious effects on serum cholesterol levels (Asadi et al., 2008). Meanwhile, Takeda et al. (2000) and Imaizumi et al. (2001) investigated the effect of long-term optional ingestion of corn oil on the caloric intake and obesity in mice (Takeda et al., 2000; Imaizumi et al., 2000). They showed that mice continued to prefer corn oil and consequently developed excessive caloric intake and obesity (Takeda et al., 2001). Investigators believe that relationship between dietary fat saturation and cholesterol metabolism is a complex matter in relation to type of dietary fat, their fatty acid composition and the level of intake (Luzfernandez et al., 1996). On the other hand, differential oil intakes of rats have been documented among high fat diet and high carbohydrate diet so that high fat diet increased their intake and preference for oil (Reed et al., 1990). Meanwhile, high fat foods such as those sold in cafeterias and supermarkets are often preferred by most people. Intake of high palatable oily or fatty foods often induces excessive caloric consumption and obesity (Takeda et al., 2001). Reports linking dietary fat to serum lipid levels have been interpreted as meaning that the general public, especially those at risk of coronary heart disease, should consume low fat diets. They argued that dietary saturated fatty acids elevated serum cholesterol concentrations, whereas polyunsaturated fatty acids reduced serum cholesterol
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concentrations and mono-unsaturated have little or no effect (KrisEtherton and Fosmire, 1984; Beynen et al., 1987a; Mattson and Grundy, 1985). Changes in the cellular cholesterol status and HDL-C values in response to different parameters have been discussed by some investigators. In this regard, the enhancing effect of exercise on HDL-C concentration has been documented (Durstine et al., 2001). In this respect, Sviridov et al., (2003) showed that additional sources of HDL-C might be derived from exercising muscle as other lipids are utilized for fuel (Sviridov et al., 2003). Moreover, it is possible that when cells become depleted of triglyceride, cellular cholesterol is also mobilized and released to its primary acceptor, HDL (Sviridov et al., 2003). Kiens and Lithell (1989) attributed post exercise increase in HDL-C concentrations to degradation of VLDL. Interestingly, Ruys et al. (1989) showed an increase in HDL production in the exercising forearm of individual who had eaten a fat meal. It has been shown that oils will be preferentially ingested by rats according to their flavors (Takeda et al., 2000; Ackroff et al., 1990). Therefore, the aim of this preliminary study was to compare the contribution of long-term optional ingestion of different vegetable oils (canola, grape seed and corn) and yogurt butter on the serum cholesterol status and the cholesterol levels in the liver and muscle in rats.
2. Materials and methods Twenty-five Wistar rats (224.83 ± 31.93 g) were purchased from the Pasteur Institute (Tehran, Iran). All rats were acclimatized in the animal house (12-h light: 12-h dark at 22 ± 2 °C) for 10 days and received a regular chow diet. Diets were purchased from Dam Pars Company (Tehran, Iran). After the acclimation period rats were randomly categorized to five groups of five rats each. Each group was maintained in a separate cage. Each cage was equipped with two bottles of water and oil except the control group (only water). Treatment groups of canola oil, grape seed oil, corn oil and yogurt butter optionally drank 100% of canola oil, grape seed oil, corn oil and yogurt butter for 10 weeks, respectively. Canola oil (C16:0, 4%; C18:0, 2%; C18:1, 62%; C18:2, 22%; C18:3, 10%), corn oil (C16:0, 11%; C18:0, 2%; C18:1, 28%; C18:2, 58%; C18:3, 1%) and grape seed oil (C16:0, 8%; C18:0, 4%; C18:1, 15%; C18:2, 73%) were purchased as commercial grade. Cow’s yogurt butter was prepared from previous day’s yogurt. Cows were reared in southwestern Iran (Bagh Malek, Khozestan, Iran). In this regard, cow’s milk yogurt from the previous day’s yogurt was churned for about 1 h, butter fat collected and gently heated to melt and formed into butter. In turn we centrifuged it for collecting the pure butter. Yogurt butter prepared, aliquoted and freezed at 80 °C until use. All procedures involving animals were approved by the Animal Care Association of the Department of Basic Sciences, School of Veterinary Medicine, University of Tehran (Tehran, Iran). Fatty acid profiles of Yogurt butter were determined by using a gas chromatograph (Agilent 6890, Oilseed Research and Development Company, Tehran, Iran) equipped with a BPX-&) column (12 m, 25 lm i.d., 0.2 lm film thickness). The column temperature was held at 45 °C for 4 min, increased to 175 °C at a rate of 13 °C/ min, to 215 °C at 4 °C and held for 60 min. Fatty acid methyl esters were identified on the basis of ISO 5508 (ISIRI 4090) and analyzed according to the ISO 5509 (ISIRI 4091). At the end of 10 weeks, rats were exsanguinated through cardiac puncture after a 12-h fast (water ad libitum). Serum concentrations of total cholesterol (TC) were measured using the cholesterol oxidase p-aminophenazone method. High density lipoprotein cholesterol (HDL-C) concentrations were measured by precipitation of apoB-containing lipoprotein with manganese-heparin and measurement of cholesterol in the supernatant according to the method of Burstein et al. (1970) with reagents prepared by Research Company (Anzan Chimie Mandegar Company, Tehran, Iran). Low density lipoprotein cholesterol (LDL-C) concentrations were measured using prepared reagents according to manufacturer instruction and calibrated with the calibrator provided by the manufacturer (Pars Azmun Company, Tehran, Iran). The livers were extracted and lipid extraction was done according to the Hara and Radin (1978) method. Briefly, in a test tube, 0.5 g of liver tissue was weighed and 9 mL of hexane:isopropanol (3:2) was added. Glass beads (2.5 mm diameter) were then added to each tube and shaken overnight. This mixture was then centrifuged at 1000g for 15 min and the supernatant was removed, mixed with 12 mL of aqueous Natrium sulfate (6.6%) and decanted for 15 min. The supernatant was then removed, dried and reconstituted in 1.5 mL of isopropanol for lipid analysis. TC of liver was estimated by the enzymatic method for each animal. Leg muscle samples were chopped and minced with mortar and pestle. An aliquot (1 g) of the sample was taken for lipid extraction and TC measured for each animal as mentioned for liver, previously.
The arrangement of data and the calculation of the mean and SD for each value was done in Microsoft Excel 2007. For each parameter, statistical analysis were done by one way ANOVA among groups using Sigma Stat 2.0 (Systat Software Inc., Point Richmond, CA). Alpha in all cases was 5% (p < 0.05).
3. Results Yogurt fatty acid profiles are tabulated in Table 1. Saturated fatty acids C16:0, C14:0 and C18:0 constitute the major fatty acids of yogurt butter. Table 2 shows oil and feed intake of rats. Rats showed a significant preference for vegetable oil intake compared to yogurt butter (p < 0.001). However, there was not any difference among vegetable oils. On the other hand, all treatment groups showed significant decrease in feed intake when compared to the control (p < 0.001). Serum TC, HDL-C and LDL-C concentrations are tabulated in Table 2. While canola oil and corn oil made decreased (about 36% and 21%, respectively) serum TC levels, significant changes were not shown in other groups when compared to the control. However, we have shown a trend to decrease in serum TC levels in all groups when compared to the control. Interestingly, while vegetable oils had any effect on the serum HDL-C concentrations, yogurt butter made a significant increase (about 122%) in serum HDL-C concentrations compared to the control (p < 0.001). Furthermore, yogurt butter decreased LDL-C concentrations (about 62%), conversely. On the other hand, a decrease in LDL-C values (about 64%) was shown for canola oil. While the amount of feed yogurt butter is not comparable with the amount of feed vegetable oils, optional intake of yogurt butter made a significant increase in the muscle TC levels (p < 0.001) and decreased liver TC levels when compared to the control (p = 0.026). In this respect, vegetable oils had no effect on the muscle and liver TC levels, except grape seed oil which decreased liver TC as much as yogurt butter. In spite of these changes, BMI scores showed the same status in all treatment groups. 4. Discussion In the present study, rats were given vegetable oils and yogurt butter solution as an optional supplement to their regular chow. Rats showed preference for optional ingestion of vegetable oils than yogurt butter. However, optional ingestion of these oils and fat made a significant decrease in feed intake. Takeda et al. (2001) argued that this condition is due to excess caloric intake in rats. Interestingly, we have shown that this increase in caloric intake is concomitant with an increase in the muscle TC and serum HDL-C values and a decrease in liver TC and LDL-C values due to
Table 1 Fatty acid composition of yogurt butter. S-SCFA (%)
S-MCFA (%)
S-LCFA (%)
Un-saturated FA (%)
C4 (2.70) C6 (2.53) C8 (1.79) C10 (4.13) C12(4.85)
C14 (14.98) C15 (1.69) C16 (38.88) C17(0.80)
C18 C20 C22 C21 C24
C10:1 C14:1 C16:1 C17:1 C18:1 C18:1 C18:2 C18:2 C20:1 C20:2 C21:1
(11.72) (0.65) (0.23) (0.10) (0.04)
(0.47) (2.29) (3.58) (0.36) trans (2.06) Cis (2.06) trans (0.34) Cis (3.36) (0.19) (0.09) (0.10)
Values were expressed as percent by weights. SCFA, saturated-short chain fatty acid; S-MCFA, saturated medium chain fatty acid; S-LCFA, saturated long chain fatty acid.
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Table 2 Serum cholesterol (TC), high density lipoprotein cholesterol (HDL-C), low density lipoprotein cholesterol (LDL-C), body mass index (BMI), liver TC, muscle TC, feed intake and oil and fat intake after 10 weeks of optional intake of different vegetable oils (canola, grape seed, corn) and yogurt butter in the corresponding rat groups (n = 5). Values were expressed as mean ± SD. Values of each parameter compared among groups using one-way ANOVA. Group
TC (mg/dl)
HDL-C (mg/dl)
LDL-C (mg/dl)
Liver TC (mg/g liver)
Muscle TC (mg/g liver)
10 Weeks Feed intake (g)
10 Weeks oil and butter intake (g)
BMI (kg/m2)
Control (I) Canola oil (II) Grape seed oil (III) Corn oil (IV) Yogurt butter (V) p-Values (differences among groups)
70.19 ± 9.64 45.03 ± 6.79 59.60 ± 10.44 55.81 ± 6.51 64.23 ± 9.74 I, II (<0.001); I, IV(0.017); II, V(0.002); II, III(0.016);
19.07 ± 3.51 16.75 ± 2.70 14.59 ± 2.49 18.26 ± 3.24 42.34 ± 9.98 I, V; II, V; III, V; IV, V (<0.001)
30.96 ± 6.38 11.28 ± 1.75 28.06 ± 6.41 22.86 ± 6.10 11.68 ± 2.06 I,II (<0.001); I, V(<0.001); I, IV(0.019); II, III(<0.001); III, (<0.001); II, IV(<0.00); IV, V(<0.001)
2.43 ± 0.31 2.74 ± 0.41 1.77 ± 0.74 2.50 ± 0.42 1.75 ± 0.31 I, III(0.037); I, V(0.032); II, V(0.003); II, III(0.004); IV, V(0.019); III, IV(0.022)
0.94 ± 0.14 0.93 ± 0.07 0.91 ± 0.15 0.91 ± 0.11 1.85 ± 0.32 I, V; II, V; III, V; IV, V (<0.001)
115.61 ± 18.32 87.15 ± 12.18 89.61 ± 12.49 90.63 ± 17.81 94.52 ± 11.82 I, II(0.006); I, III(0.012); I, IV(0.015); I, V(<0.001)
0 6.84 ± 1.93 7.34 ± 2.31 7.11 ± 1.61 1.91 ± 0.74 II, IV; III, V; IV, V (<0.001)
5.74 ± 0.51 5.74 ± 0.33 5.73 ± 0.73 5.97 ± 0.78 5.92 ± 0.42 No
the optional ingestion of yogurt butter. This beneficial effect of yogurt butter may be due to applied yogurt butter production process. In the present study we used a manually produced unpurified butter. It seems that this procedure is less harmful for useful compounds of yogurt butter compared to the manufacturing procedure. In line with our findings, Tholstrup et al. (2004) declared that some hypocholesterolemic factors associated with some milk products may be removed during the butter production process. Furthermore, the effect of regular intake of milk fat on the lipid and lipoprotein metabolism has been discussed by Haug et al. (2008). They argued that the moderate intake of milk fat may reduce the risk of atherosclerotic diseases due to a reduction in small dense low density lipoprotein particles. This property of the milk fat can be attributed to its conjugated linoleic acid ingredients (Haug et al., 2008). Hence, this can be deduced that milk contains a beneficial milk factor which somehow modulates the cholesterol raising effect of the milk fat. As can be seen in Table 1, saturated and mono-unsaturated fatty acids constitute the major components of yogurt butter. Therefore, these favorable effects cannot be attributed to its polyunsaturated fatty acids as is right in vegetable oils. This hypothesis is in line with a finding that whole milk reduces plasma and hepatic TG in rats. This condition has been discussed with some investigators so that they believe a high intake of whole milk is associated with a low risk of coronary artery disease in middle-aged men in a manner that cannot simply be predicted by the fat content of whole milk (Tholstrup et al., 1998). Moreover, similar status has been argued in physically active people who received dairy products by Sviridov et al. (2003). However, these investigators did not mention the required amount of exercise or dairy products on its protective effect. Our findings about the optional intake of diet supplemented with manually prepared milk fat may be a novel finding in this regard. They believe that these effects of dietary fat on cholesterol status could potentially be attributable to factors including fatty acid consumption or the presence of plant sterols or other constituents. Can these factors have an effects on the muscle TC levels? Moreover, is it possible for muscle TC to contribute in HDL-C synthesis due to the optional intake of these unpurified fat? Or is this condition is due to their effects on the hepatic pre-b HDL synthesis? All of these questions should be investigated in future studies. Chung et al. (2003) studied the effect of isoflavone and/or grape seed oil supplementation on blood lipid profiles and bone strength in ovariectomised female rats. In the present study, we have shown a significant decrease in liver TC levels due to the intake of grape seed oil and milk fat. Chung et al. (2003) found that after 8 weeks feeding of grape seed oil supplementation to rats it decreased TC, TG and LDL-C levels, yet crude lipid and TC contents in liver were
not affected in this condition. In this regard, it has been previously shown that diets rich in either olive or canola oils appeared to increase serum HDL-C concentrations. Moreover, reducing total fat calories in the diet decreased both plasma LDL-C and HDL-C concentrations (Mattson and Grundy, 1985). It has been documented that the intake of mono-unsaturated fatty acids compared with polyunsaturated fatty acids will be resulted in increased plasma cholesterol levels in rats (Kris-Etherton and Fosmire, 1984; Beynen et al., 1987b). Analysis of the canola, grape seed and corn oils showed that they are rich in mono-unsaturated fatty acid (oleic acid), linoleic acid and n-6 polyunsaturated fatty acid, respectively. Karvonen et al. (2002) showed the effect of rape seed oil based cheese (milk fat substituted by rape seed oil) on serum TC and lipoprotein lipid concentrations in reference to ordinary milk fat based cheese in subjects with mildly to moderately elevated serum cholesterol concentration. They showed that rape seed oil based cheese reduced serum TC and LDL-C concentrations in mildly to moderately hypercholesterolemic subjects when replacing ordinary milk fat based cheese in the diet. In present study, we have shown a trend to decrease in serum TC levels and a significant decrease in the levels of LDL-C in canola oil, corn oil and yogurt butter groups. However, we have not been able to show the beneficial effects of grape seed oil on HDL-C and LDL-C values when used as optional ingestion. It seems that optional grape seed oil ingestion makes its effect by changing cellular (muscle and liver) cholesterol status than the serum cholesterol parameters. Some disagreements in the findings show that the regular intake of grape seed oil has beneficial effects on serum HDL-C in human subjects. In this an respect increase in serum HDL-C levels and a decrease in LDL-C levels, TC/HDL-C and LDL-C/HDL-C ratios have been reported. They have shown that up to 45 g intake of grape seed oil per day raised HDL-C levels by 13%, reduced LDL-C levels by 7%, decreased TC/HDL-C ratio by 15.6% and reduced LDL-C/HDL-C ratio by 15.3% in 3 weeks (Uma Maheswari and Rao, 2005; Nash, 2004). The present report revealed that optional supplement of canola oil to the normal diet reduced serum TC concentrations with respect to the control. Such a status can be attributed to its high level of polyunsaturated fatty acids in combination with mono-unsaturated fatty acids.
5. Conclusion It seems yogurt butter has some beneficial factors for changing serum and liver cholesterol status. These preliminary findings would be investigated in future for checking the effect of different
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