Differential Effects of Fatty Acids and Exercise on Body Weight Regulation and Metabolism in Female Wistar Rats

Abstract

High-fat diets made with different fats may have distinct effects on body weight regulation and metabolism. In the present study, the metabolic effects of high-fat (HF) diets made with fish oil, palm oil, and soybean oil were compared with a low-fat diet in female Wistar rats that were either exercised (EX, swimming) or that remained sedentary as controls. Each adult rat was exposed to the same diet that their dams consumed during pregnancy and lactation. When they were 9 weeks old, rats began an EX regimen that lasted for 6 weeks. Twenty-four hours after the last EX bout, rats were sacrificed in a fasted state. It was observed that HF feeding of soybean oil induced more body weight and fat gain, as well as insulin resistance, as indicated by insulin/glucose ratios, than other oils. Female rats fed a HF diet made with fish oil had body weight and insulin sensitivity not different from that observed in low fat fed control rats. For rats fed HF diets made with soybean oil or palm oil, EX also exerted beneficial effects by reducing body fat %, blood insulin, triglyceride and leptin levels, as well as improving insulin sensitivity.

It is well established that diets high in fat content induce rapid weight gain, obesity, and insulin resistance in rats (1, 2), mice (3, 4), and humans (5, 6). It has also been reported that different types of fatty acids have different effects on body weight gain and insulin resistance. Saturated fatty acids (SFAs) produce more weight gain and insulin resistance than polyunsaturated fatty acids (PUFAs) in some studies (7–12). However, Hill et al. reported more weight gain in rats fed PUFAs than those fed SFAs (13). Of all the PUFAs, long-chain PUFAs (LCPUFAs), such as arachidonic acid (20:4, n-6), eicosapentanoic acid (EPA, 20:5, n-3), and docosahexenoic acid (DHA, 22:6, n-3), exert a more favorable influence on both body weight and metabolic profile compared with other n-6 PUFAs (14, 15). Mice fed soybean oil (mainly n-6 PUFAs) or palm oil (mainly SFAs) gained more weight than mice fed a fish oil diet (mainly n-3 PUFAs; Ref. 4). High intake of linoleic acid also increased fasting blood glucose levels (4). Borkman et al. (16) have reported that blood insulin concentration (an indicator of insulin resistance) was negatively correlated with LCPUFA content in muscle. Dietary linoleic acid (18:2, n-6) content, however, is positively associated with blood insulin levels, and it may impair insulin action in animals and humans (4, 17). Partial replacement of the linoleic acid with fish oil (n-3 PUFAs) prevents the onset of insulin resistance (14). Countries with high linoleic acid intake, such as Israel, suffer the highest rate of insulin resistance, Type II diabetes, and cardiovascular diseases (18). SFAs are also known to induce insulin resistance, especially in obese humans (19, 20). Thus, not all fatty acids produce the same effects on body weight regulation and metabolism. High intakes of linoleic acid or SFAs may not be beneficial.

Exercise is commonly recommended to obese patients to reduce body weight gain and insulin resistance (21–23). Exercise also reduces the adverse effects of dietary fat on insulin levels in women (17) and improves insulin sensitivity in high fat fed animals (23).

The interaction of dietary fatty acid composition and exercise on body weight regulation and insulin resistance has not been thoroughly investigated. Bell et al. (24) reported that voluntary exercise reduced body fat in mice fed a low fat diet or high fat diets made with beef fat or canola oil without any change in lean body mass. However, beef fat induced more body fat gain in both exercised and nonexercised mice compared with low-fat and canola oil-fed mice. Thus, the quantity of the fat in the diets as well as the type of fats used will affect the body weight regulation. Considering the fact that soybean oil consumption has increased from less than 2 billion pounds in 1950 to 12 billion pounds in 1995–1996 (25), the effects of soybean oil consumption on body weight regulation and metabolism need to be examined. The present study was designed to test the hypothesis that different fatty acids would interact differently with exercise on body weight regulation in female Wistar rats.

Materials and Methods

Animals.

Wistar female offspring from dams obtained from Harlan Sprague-Dawley (Indianapolis, IN) were the subjects of this study. The dams were fed either a control low fat diet (CON) or one of the three high-fat diets (HF, 40% by weight) starting 1 week before mating. The dams were continuously fed the same diet for the entire gestation and lactation period. Within 24 hr after delivery, pups were counted, weighed and length measured. Postnatal litter size was maintained at 10 pups per litter, with five male and five female pups whenever possible. Weaning occurred on Day 21 of lactation. After weaning, two male and two female pups from each litter were housed in individual cages. To avoid introducing different prenatal, preweaning, and postweaning diet effects, all offspring were fed the same diet that was fed to their dams ad libitum. These offspring were followed into adulthood. When they were 9 weeks old, a fasting blood sample was obtained from the retro-orbital sinus of each rat for glucose, insulin, and triglyceride (TG) determinations. After this blood sampling, they were then divided into two groups within each diet group: control sedentary (SD) and exercise (EX). One male and one female rat from each litter were trained to exercise, and the remaining ones were maintained as sedentary. The study procedure was approved by the Animal Investigation Committee of Wayne State University.

Diets.

Four diets were used in this study and were prepared by Dyets Inc (Bethlehem, PA). The low-fat control diet (CON) diet was formulated based on the AIN-93G formula (26). The three HF diets were similar in composition except for the fats used: fish oil (FO), palm oil (PO), and soybean oil (SO). The caloric distribution of carbohydrate, protein, and fat of the CON and HF diets are: 63.4%, 20.7%, 15.9% and 15.2%, 19.4%, 65.4%, respectively. With the higher caloric density in the HF diets, rats usually reduce the amount of food eaten daily. To assure that rats are not protein, mineral, or vitamin deficient, extra protein, minerals, and vitamins were added at the expense of carbohydrate. FO (Menhaden oil) is low in linoleic acid, a required fatty acid for normal growth (26). Therefore, the FO diet was made with 70 g of SO plus 330 g of FO to ensure adequate intake of linoleic acid for growth. A similar adjustment was made to the PO diet. The diet composition for the four diets is listed in Table I. The final four exercised and four sedentary groups were: CONEX, CONSD, FOEX, FOSD, POEX, POSD, SOEX, and SOSD.

Exercise.

Swimming was the exercise regimen used in this study. Rats were trained to swim in a 30-gallon barrel of lukewarm water, starting when they were 9 weeks old. Hot water was added between groups of rats if the water temperature became cold. Training was accomplished in 2 weeks: the first day started with a 15 min swim and was gradually increased to 2 hr per day, 5 days per week. Rats were continuously monitored during swimming to prevent them from drowning. At the end of each daily swimming session, each rat was dried and placed by a heating lamp until their fur was completely dry before rats were returned to their cages. The entire exercise duration was 6 weeks. The SD rats remained in their cages during this exercise period.

Sacrifice Procedure.

At the completion of 6 weeks of swimming, rats were fed ad libitum for 24 hr. They were then fasted overnight and sacrificed by decapitation following a brief exposure to CO₂. Trunk blood was collected, centrifuged and plasma was stored for later assays. Livers were removed, weighed and submerged in liquid nitrogen before being stored in a −70°C freezer for assays later. All visible fat in the abdominal cavity was collected, weighed, and was designated as internal fat. The body was eviscerated and stored in a freezer for body composition analysis at a later date. Sedentary rats were sacrificed at the same time as the exercised rats.

Biochemical Assays.

Blood Parameters.

Blood glucose levels were analyzed by the method of Trinder (27), TG levels were assayed using a kit purchased from Sigma Chemical Co. (St. Louis, MO) using the method of Bucolo and David (28), and insulin levels were determined by radioimmunoassay using a kit from ICN Biomedicals, (Costa Mesa, CA). Plasma leptin concentrations were measured using a rat leptin kit purchased from Linco Research (St. Charles, MO).

Liver Parameters.

Liver glycogen was measured using the techniques described by Lo et al. (29). Liver lipid levels were measured using the method of Folch et al. (30).

Body Composition.

Body composition was determined on eviscerated and shaved carcass according to the procedure described by Jen et al. (31). Triplicate homogenate samples were used to measure lipid and water content. The lipid determined from body composition analysis was designated as subcutaneous fat content. Internal fat and subcutaneous fat contents were added together to represent the total fat content in each rat.

Statistical Analysis.

All data are presented as mean ± standard error of means (SEM). Analyses of variance were performed on blood glucose, TG and insulin levels, liver glycogen and lipid contents, and total and percent body fat. Analyses of variance with repeated measures were used to compare the group difference in body weight over the entire study period. GB-STAT software (Dynamic Microsystems, Inc., Silver Springs, MD) was used for statistical analysis. Significance level was set at P < 0.05.

Results

Baseline Data.

Before the beginning of exercise regimen, rats fed the PO and SO diets weighed significantly more than CON and FO fed rats (Table II). There was no difference among the four diet groups in blood glucose, insulin, and TG levels.

Effects of Diet.

Food Intake, Body Weight, and Composition at Sacrifice.

For the entire study period, the CONSD, FOSD, and SOSD rats had similar caloric intakes and, all were significantly lower than that of the POSD rats (CONSD: 2821 ± 100 kcal; FOSD: 2938 ± 134; POSD: 3367 ± 125; SOSD: 2869 ± 118; P < 0.01). Despite the similarity in caloric intake, body weights separated into two groups, with CONSD and FOSD rats having lower body weights than POSD and SOSD rats (Table III ).

Diet had significant effects on body fat content (P < 0.01). SOSD rats were fatter than all other groups in subcutaneous fat % and total fat % (Table III ), but SOSD rats had similar internal fat % and total fat mass as the POSD rats. Female rats fed a HF diet made with FO had similar amount of total fat %, internal fat % and subcutaneous fat % as the low fat fed controls.

Blood Parameters at Sacrifice.

Insulin and Glucose Levels.

Diet exerted a significant effect on blood insulin levels. Blood insulin levels in SOSD rats were significantly higher (P < 0.05) than that of the CONSD and FOSD groups but were not different from that of the POSD rats (Table IV ). FOSD rats had insulin levels that were similar to the CONSD rats but were lower than that of the POSD rats. Diets did not affect blood glucose levels.

Insulin/Glucose (I/G) Ratios.

Fasting I/G ratio was calculated as an indicator for insulin resistance since this index has been shown to be a good indicator for insulin sensitivity (32, 33). The SOSD group had significantly higher I/G ratios than that of the FOSD group (P < 0.05). SOSD group had I/G levels not different from CONSD and POSD groups while CONSD, FOSD and POSD groups had similar levels.

TGs.

FOSD rats had significantly lower TG levels than that of the CONSD and SOSD groups (P < 0.01) but not different from the POSD group. TG levels in CONSD, POSD, and SOSD groups were similar.

Leptin Levels.

FOSD rats had similar leptin levels as the other three groups. Leptin levels of POSD and SOSD groups were similar and were significantly higher than the CONSD group (P < 0.05). Because HF fed rats also had higher body fat, leptin was corrected for body fatness. After this adjustment, there was no difference in leptin/g fat tissue among the four groups.

Liver Parameters.

HF-fed rats had heavier livers than low fat fed control rats (Table V). POSD had similar liver weight compared with FOSD and SOSD. However, FOSD had higher liver weights compared with SOSD. FOSD rats had the highest liver lipid concentration and content, although it was not significantly different from that of the POSD rats. Liver lipid concentrations and content were similar in CONSD, POSD, and SOSD rats. Liver glycogen concentrations were significantly higher in POSD rats compared with that of the CONSD and FOSD rats. CONSD, FOSD, and SOSD groups had similar liver glycogen concentrations. POSD also had a higher amount of total liver glycogen than that of the CONSD and FOSD group, but it was not different from that of the SOSD group.

Effect of EX.

Food Intake, Body Weight, and Composition.

Although EX reduced body weight in all four groups of female rats, the reduction in body weight was not significant (Table III ). When body weight changes during the EX period were compared (difference between baseline and sacrifice weight), it was revealed that EX reduced weight gain in PO and SO groups but not in CON and FO groups (data not shown). EX significantly reduced internal fat % because of the reduction in CONEX and POEX groups, whereas the SOEX and FOEX groups did not show a significant reduction. CONEX, POEX and SOEX groups all showed a significant decrease in subcutaneous fat %. Nevertheless, SOEX rats still had significantly higher subcutaneous fat % compared with the other three groups. EX reduced total body fat mass, especially in POEX and SOEX groups, although these two groups still had more body fat mass than the CONEX and FOEX groups. Total body fat % was also reduced by EX in CONEX, POEX and SOEX groups. The POEX rats had similar total body fat % compared with CONEX and FOEX, while SOEX rats had significantly higher total fat % than all the other groups.

Blood Parameters.

Insulin and Glucose Levels.

Table IV shows the blood parameters assessed in this study. EX significantly reduced blood insulin levels. More specifically, it normalized the hyperinsulinemia observed in rats fed the PO and SO diets; thus, all four diet groups had similar insulin levels. Blood glucose levels were not affected by EX and all four EX groups had similar blood glucose levels.

I/G Ratios.

EX improved I/G ratios, and significantly lowered the I/G ratios in the SOEX group compared to its sedentary counterpart. Thus, all four EX groups had similar I/G ratios.

TGs.

EX reduced blood TG significantly. POEX rats had significantly higher TG levels than that of the FOEX rats, but both groups were not different from the other two groups.

Leptin Levels.

Blood leptin levels were significantly reduced by EX, especially in FOEX and POEX groups. SOEX rats did not show such reduction and still had significantly higher blood leptin levels than that of the CONEX and FOEX rats. When leptin levels were adjusted for body fat content, a significant reduction in leptin/g fat tissue was still apparent. This reduction by EX was observed in CONEX and POEX groups. SOEX rats still had levels higher than the CONEX and FOEX rats, but not different from the POEX rats.

Liver Parameters.

EX did not affect liver weight or liver lipid parameters. Liver glycogen concentration and content were significantly elevated by EX, especially in FOEX and SOEX groups compared with the CONEX and POEX groups (Table V ).

Discussion

This study demonstrated that dietary fatty acids had different effects on body weight regulation in HF-fed female rats. The effects of HF FO feeding were similar to those of the CON low-fat diet. It induced less weight or fat gain compared to other HF diets. SO feeding, however, induced the highest weight and fat gain of all oils given. Rats fed the PO diet had body weights that were not different from SO rats, but PO rats had significantly lower fat % than SO-fed rats. Ikemoto et al. observed that HF diets made with SO induced the most weight gain whereas FO induced the least in mice (4). It has also been reported that dietary lipid uptake in retroperitoneal and epididymal fat pads was increased in SO fed rats compared with FO or FO plus SO-fed rats (34). Fickova et al. (35) observed similar results and concluded that increased lipolysis and reduced glucose uptake by fat cells by FO feeding were the mechanisms for the reduced weight gain.

Saturated fatty acids have been reported to produce more weight gain and obesity in some studies (7, 12, 36). However, it also has been reported that n-6 PUFAs induce more weight gain (13), increase fat cell number, and amplify hepatic lipogenic enzyme activities compare to that seen with SFAs (37). The types of PUFA used, the quantity of fat in the diets, and the length of time studied are just a few of the factors that may affect study results. A diet high in FO content more consistently reduces weight gain relative to other types of fats/oils (38–40).

One of the possible mechanisms responsible for the differential effects of fatty acids on weight gain may be related to the rates of oxidation. Leyton et al. (41) reported that rats fed fatty acids of different chain length and saturation showed varied oxidation rates, with SFAs showing the least oxidation and PUFA showing higher oxidation rates. For PUFAs, linolenic acid is oxidized more efficiently than that of linoleic acid (42, 43). Fatty acid oxidation rates are inversely related to fat storage, with the higher the oxidation, the lesser the body fat accumulation.

It is well established that HF feeding in animals induces insulin resistance (1, 3, 15). In the current study, we used the I/G ratio as a measure of insulin resistance (32, 33). Our findings indicate that different dietary fatty acids have distinct influence on I/G ratios and thus insulin resistance. FO-fed female rats had lowest blood TG levels and highest insulin sensitivity, as indicated by the lowest I/G ratios when compared with all other groups. SO fed rats showed hyperinsulinemia compared with both FO-fed rats and low fat-fed rats. It is known that high n-3 PUFA or high n-3/n-6 ratios in diet improves insulin action (14). Dietary fatty acid composition is significantly correlated to cell membrane fatty acid composition (12). The higher the degree of unsaturation in muscle membrane fatty acid composition, the higher the insulin sensitivity has been reported (15). n-3 fatty acids of fish oils are known to be elongated and are desaturated to a greater extent than n-6 fatty acids (43), producing a higher unsaturation index in FO-fed rats. FO may also reduce insulin resistance in HF-fed rats by reducing circulating TG levels (37, 44, 45), a phenomenon also observed in the present study. A reduced TG level in turn reduces the accumulation of TGs in muscle and reduces insulin resistance (46). These reasons may partially explain the higher insulin sensitivity in FO-fed rats. In contrast, linoleic acid, the major fatty acid in soybean oil, has been shown to impair insulin action in animals (4) and humans (17) when consumed in large amounts. Our data clearly support the notion that SO may cause insulin resistance in rats fed the HF diet made with this oil. Similar results have been reported by others using n-6 PUFA diet. High safflower oil diet decreased 2-deoxyglucose uptake in adipose tissue as compared to that in HF diet made with mixed oils (47).

Even though SO fed rats weighed more and were more insulin resistant than rats fed the FO diet, the insulin resistance was improved after the exercise regimen. Physically active women were reported to have improved insulin action, even with a high consumption of linoleic acid and after adjusting for obesity (17).

EX in female rats induced a significant reduction in blood TG levels. This reduction in TG levels could have made these rats more insulin sensitive (48). This enhanced insulin sensitivity may account for the increased glycogen store in the livers of exercised rats. The reduction in blood TG levels, an increased utilization of fat as an energy source during EX, and a reduction in body fat make EX an ideal means to improve body weight and composition, as well as blood lipid profiles, in female animals, and potentially in humans.

After EX, female rats showed a 55% reduction in blood leptin levels. This reduction is independent of the reduction of body fat because leptin levels per gram of fat tissue was still lower in exercised rats. Hickey et al. have reported that in female humans, exercise lowered blood leptin levels even though body fat mass was not reduced (49). With reduced leptin levels, leptin sensitivity may be restored. Thus EX may make weight maintenance easier in female animals or humans. The results also indicated that the effect of EX on leptin sensitivity may be dependent on the dietary fat source, because leptin per gram of fat was reduced only in PO-fed rats, but not in SO- or FO-fed rats.

In conclusion, this study demonstrated that not only the quantity but also the quality of dietary fat affects body weight regulation and metabolic profile. A diet high in linoleic acid, found in soybean oil, did induce more body weight and fat gain as well as insulin resistance compared to FO and CON diets in the present study. FO, even in high amounts, did not induce obesity and insulin resistance, thus EX did not exert further beneficial effects in these two parameters. EX attenuated the induction of insulin resistance, as well as the gains in body weight and fat by a HF diet composed of SO and PO in female rats. However, body fat % was still greater in rats fed SO than those fed PO after EX, which may be related to the fact that EX did not significantly reduce leptin per gram of fat levels in SO fed rats. Further study to examine whether this is the result of an actual reduction in leptin sensitivity by SO feeding relative to other oils by measuring leptin expression is warranted.

Table I.

Diet Composition of Four Diets Used in This Study (g/kg)

Ingredients	CON	FO	PO	SO
^a Deytrose, Dyets, Inc., Bethlehem, PA.
Casein (80 mesh)	200	260	260	260
Cornstarch	321.84	6.51	6.51	6.51
Maltodextrin^a	107.28	2.17	2.17	2.17
Maltose dextrin	200	200	200	200
Cellulose	50	65	65	65
Soybean oil	70	70	70	400
Menhaden oil (fish oil)	—	330	—	—
Refined palm oil	—	—	330	—
t-butylhydroquinone	0.08	0.08	0.08	0.08
Salt mix	35	45.5	45.5	45.5
Vitamin mix	10	13	13	13
Vitamin E acetate	0.3	0.39	0.39	0.39
L-Cystine	3.0	3.9	3.9	3.9
Choline bitartrate	2.5	3.25	3.25	3.25
Energy content (kcal/g)	3.97	5.50	5.50	5.50
Percent by calorie
Carbohydrate	63.4	15.2	15.2	15.2
Protein	20.7	19.4	19.4	19.4
Fat	15.9	65.4	65.4	65.4

Table II.

Baseline Body Weight and Blood Parameters Before the Commencement of Exercise

	n	Body weight (g)	Insulin (μU/ml)	Glucose (mg/dl)	I/G	Triglyceride (mg/dl)
Numbers with different superscripts within each column are significantly different from each other at P < 0.05 or 0.01.
CON, control low fat diet; FO, fish oil; PO, palm oil; SO, soybean oil.
CON	15	340 ± 13^a	71.6 ± 9.9	111 ± 9	0.68 ± 0.05	29 ± 5.7
FO	21	324 ± 11^a	49.1 ± 3.5	102 ± 7	0.51 ± 0.05	19 ± 3.5
PO	16	384 ± 11^b	53.5 ± 4.9	107 ± 8	0.54 ± 0.05	27 ± 6.9
SO	18	374 ± 12^b	55.7 ± 6.0	119 ± 9	0.50 ± 0.12	19.6 ± 4.3

Table III.

Body Weight and Composition of Rats at Sacrifice

	n	Body wt (g)	Internal fat %	Subq fat %	Total fat (g)	Total fat %
Numbers with different superscripts within each column are significantly different from each other at P < 0.05 or 0.01.
* EX and SD groups of the same diet were significantly different from each other.
CONSD, low fat, sedentary; FOSD, fish oil, sedentary; POSD, palm oil, sedentary; SOSD, soybean oil, sedentary; CONEX, low fat, exercised; FOEX, fish oil, exercised; POEX, palm oil, exercised; SOEX, soybean oil, exercised.
CONSD	7	377 ± 19^a	9.6 ± 1^a	10.5 ± 1.0^a	79.8 ± 11.9^a	20.2 ± 2.0^a
FOSD	11	396 ± 14^a	9.5 ± 0.5^a	11.1 ± 0.9^a	80.1 ± 6.8^a	20.3 ± 1.1^a
POSD	8	451 ± 16^b	13 ± 0.7^b	14.1 ± 1.0^b	124.4 ± 11.9^b	27.2 ± 1.6^b
SOSD	9	466 ± 20^b	13 ± 0.6^b	17.2 ± 1.2^c	137.1 ± 10.3^b	30.2 ± 1.5^c
CONEX	8	364 ± 10^a	7.6 ± 0.7^a*	7.8 ± 0.5^a*	53.4 ± 4.3^a	15.0 ± 1.2^a*
FOEX	9	371 ± 9^a	9.0 ± 1.1^a	9.7 ± 0.3^a	63.5 ± 4.6^a	17.0 ± 1.0^a
POEX	8	413 ± 21^a ^b	8.5 ± 1.1^a*	9.9 ± 1.5^a*	82.6 ± 15.6^b*	18.9 ± 2.6^a*
SOEX	8	442 ± 27^b	11.8 ± 0.9^b	13.1 ± 0.9^b*	102.9 ± 9.5^b*	24.3 ± 1.6^b*
EX	33	396 ± 10	8.7 ± 0.5^a	10.0 ± 0.5^a	73.7 ± 5.3^a	18.5 ± 1.0^a
SD	35	421 ± 10	11.2 ± 0.4^b	12.9 ± 0.7^b	101.5 ± 6.6^b	23.8 ± 1.1^b

Table IV.

Blood Parameters of all Four Diet Groups as Well as Exercise and Nonexercise Subgroups of Rats at Sacrifice

	Insulin (uU/ml)	Glucose (mg/dl)	I/G	TG (mg/dl)	Leptin (ng/ml)	Leptin (ng/g fat)
Numbers with different superscripts within each four groups are significantly different from each other at P < 0.05 or 0.01.
* EX and SD groups of the same diet were significantly different from each other.
CONSD, low fat, sedentary; FOSD, fish oil, sedentary; POSD, palm oil, sedentary; SOSD, soybean oil, sedentary; CONEX, low fat, exercised; FOEX, fish oil, exercised; POEX, palm oil, exercised; SOEX, soybean oil, exercised.
CONSD	58.7 ± 6.6^ab	138 ± 12	0.46 ± 0.04^ab	45 ± 4.7^a	6.8 ± 1.8^a	0.087 ± 0.011
FOSD	51.8 ± 3.7^b	140 ± 6	0.37 ± 0.03^a	28 ± 5^b	10.1 ± 2.2^ab	0.087 ± 0.010
POSD	74.8 ± 8.3^ac	158 ± 12	0.46 ± 0.03^ab	44 ± 4^ab	16.1 ± 2.9^b	0.125 ± 0.013
SOSD	85.5 ± 10^c	156 ± 11	0.58 ± 0.08^b	54 ± 7.5^a	15.4 ± 2.4^b	0.120 ± 0.018
CONEX	52.4 ± 6.7	134 ± 18	0.44 ± 0.04	31 ± 4.3^ab	2.7 ± 0.3^a	0.050 ± 0.004^a*
FOEX	51.5 ± 2.5	159 ± 14	0.35 ± 0.04	18 ± 5^b	4.0 ± 0.8^a*	0.058 ± 0.008^a
POEX	59.7 ± 7.8	153 ± 16	0.42 ± 0.05	50 ± 10^a	5.8 ± 1.7^ab*	0.073 ± 0.009^ab*
SOEX	57.3 ± 4.7	156 ± 10	0.37 ± 0.02*	32 ± 3.7^ab	9.2 ± 2.3^b	0.091 ± 0.018^b
EX	55.0 ± 2.8^a	151 ± 8	0.39 ± 0.03^a	32 ± 4^a	5.1 ± 0.8^a	0.066 ± 0.006^a
SD	68.1 ± 4.4^b	148 ± 5	0.47 ± 0.03^b	42 ± 3.2^b	11.4 ± 1.3^b	0.102 ± 0.007^b

Table V.

Liver Glycogen and Lipid Content of Four Diet Groups as Well as Exercise and Nonexercise Subgroups of Rats at Sacrifice

Group	Liver weight (g)	Liver lipid (mg/g)	Total liver lipid (g)	Liver glycogen (mg/g)	Total liver glycogen (g)
Numbers with different superscripts within each 4 groups are significantly different from each other at P < 0.05 or 0.01.
* EX and SD groups of the same diet are significantly different from each other.
CONSD, low fat, sedentary; FOSD, fish oil, sedentary; POSD, palm oil, sedentary; SOSD, soybean oil, sedentary; CONEX, low fat, exercised; FOEX, fish oil, exercised; POEX, palm oil, exercised; SOEX, soybean oil, exercised.
CONSD	9.7 ± 0.6^a	92 ± 7^a	0.91 ± 0.13^a	5.2 ± 1.9^a	0.05 ± 0.02^a
FOSD	14.6 ± 0.9^b	202 ± 29^bc	3.39 ± 0.76^bc	12.0 ± 3.2^a	0.19 ± 0.05^a
POSD	12.7 ± 0.7^bc	158 ± 15^ac	1.99 ± 0.33^ac	27.1 ± 7.2^bc	0.35 ± 0.10^b
SOSD	12.5 ± 0.5^c	91 ± 4^a	1.09 ± 0.02^a	17.2 ± 2.1^ac	0.21 ± 0.03^ab
CONEX	10.5 ± 0.3^a	95 ± 14	0.99 ± 0.18	9.8 ± 1.0^a	0.10 ± 0.01^a
FOEX	14.2 ± 0.9^b	170 ± 27	2.53 ± 0.56	41.1 ± 2.9^b*	0.56 ± 0.12^b*
POEX	12.5 ± 0.6^b	163 ± 16	2.03 ± 0.28	24.6 ± 7.1^a	0.32 ± 0.09^a
SOEX	12.6 ± 0.8^b	110 ± 17	1.20 ± 0.14	42.4 ± 10.9^b*	0.50 ± 0.12^b*
EX	12.4 ± 2.4	143 ± 13	1.86 ± 0.25	28.6 ± 4.3^a	0.36 ± 0.06^a
SD	12.4 ± 2.8	137 ± 16	1.90 ± 0.38	16.2 ± 2.3^b	0.21 ± 0.03^b

Footnotes

This research was supported by a grant from the Thomas Foundation, Michigan to Dr. K-L.C. Jen.

1

To whom requests for reprints should be addressed at the Department of Nutrition and Food Science, 3009 Science Hall, Wayne State University, Detroit, MI 48202. E-mail:

References

Jen K-LC. Effects of diet composition on food intake and carcass composition in rats. Physiol Behav 42 : 551–556, 1988.

Storlien LH, James DE, Burleigh KM, Chisholm DJ, Kragen EW. Fat feeding causes widespread in vivo insulin resistance, decreased energy expenditure, and obesity in rats. Am J Physiol 251 : E576–E586, 1986.

Lin S, Thomas T, Storlien LH, Huang XF. Development of high fat-induced obesity and leptin resistance in C57BL/6J mice. Int J Obes 24 : 639–646, 2000.

Ikemoto S, Takahashi M, Tsunoda N, Maruyama K, Itakura H, Ezaki O. High-fat diet-induced hyperglycemia and obesity in mice: Differential effects of dietary oils. Metabolism 45 : 1539–1546, 1996.

Thomas CD, Peters JC, Reed GW, Abumrad NN, Sun M, Hill JO. Nutrient balance and energy expenditure during ad libitum feeding of high-fat and high-carbohydrate diets in humans. Am J Clin Nutr 55 : 934–942, 1992.

Bengtsson C, Bjorkelund C, Lapidus L, Lissner L. Associations of serum lipid concentrations and obesity with mortality in women—20 year follow up of participants in the prospective population study in Gothenburg, Sweden. Br Med J 307 : 1385–1388, 1993.

Dreon DM, Frey-Hewitt B, Ellsworth N, Williams PT, Terry RB, Wood PD. Dietary fat:carbohydrate ratio and obesity in middle-aged men. Am J Clin Nutr 47 : 995–1000, 1988.

Larson DE, Hunter GR, Williams M, Kekes-Szabo T, Nyikos I, Goran MI. Dietary fat in relation to body fat and intraabdominal adipose tissue: A cross-sectional analysis. Am J Clin Nutr 64 : 677–684, 1996.

Loh MY, Flatt WD, Martin RJ, Hausman DB. Dietary fat type and level influence adiposity development in obese but not lean Zucker rats. Proc Soc Exp Biol Med 218 : 38–44, 1998.

10.

Westerterp KR, Goran MI. Relationship between physical activity related energy expenditure and body composition: A gender difference. Int J Obes 21 : 184–188, 1997.

11.

Matsuo T, Shimomura Y, Saitoh S, Tokuyama K, Takeuchi H, Suzuki M. Sympathetic activity is lower in rats fed a beef tallow diet than in rats fed a safflower oil diet. Metabolism 44 : 934–939, 1995.

12.

Pan DA, Hulbert AJ, Storlein LH. Dietary fats, membrane phospholipids and obesity. J Nutr 124 : 1555–1565, 1994.

13.

Hill JO, Lin D, Yakubu F, Peters JC. Development of dietary obesity in rats: Influence of amount and composition of dietary fat. Int J Obes 16 : 321–333, 1992.

14.

Storlein LH, Kraegen EW, Chisholm DJ, Ford GL, Bruce DG, Pascoe WS. Fish oil prevents insulin resistance induced by high-fat feeding in rats. Science 237 : 885–888, 1987.

15.

Storlien LH, Jenkins AB, Chisholm DJ, Pascoe WS, Khouri S, Karegen EW. Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglyceride and w-3 fatty acids in muscle phospholipids. Diabetes 40 : 280–289, 1991.

16.

Borkman M, Storlein LH, Pan DA, Jenkins AB, Chisholm DJ, Campbell LV. The relation between insulin sensitivity and the fatty-acid composition of skeletal-muscle phospholipids. N Engl J Med 328 : 238–244, 1993.

17.

Mayer EJ, Newman B, Quesenberry CJ Jr, Selby JV. Usual dietary fat intake and insulin concentrations in healthy women twins. Diabetes Care 16 : 1459–1469, 1993.

18.

Yam D, Eliraz A, Berry EM. Diet and disease–the Israeli paradox: Possible dangers of a high omega-6 polyunsaturated fatty acid diet. Isr J Med Sci 32 : 1134–1143, 1996.

19.

Rivellese AA, De Natale C, Lilli S. Type of dietary fat and insulin resistance. Ann NY Acad Sci 967 : 329–335, 2002.

20.

Lovejoy JC, Smith SR, Champagne CM, Most MM, Lefevre M, DeLany JP, Denkins YM, Rood JC, Veldhuis J, Bray GA. Effects of diets enriched in saturated (palmitic), monounsaturated (oleic), or trans (elaidic) fatty acids on insulin sensitivity and substrate oxidation in healthy adults. Diabetes Care 25 : 1283–1288, 2002.

21.

Ruderman NB, Schneider SH. Diabetes, exercise, and atherosclerosis. Diabetes Care 15 : 1787–1793, 1992.

22.

Ballor DL, Katch VL, Becque MD, Marks CR. Resistance weight training during caloric restriction enhances lean body weight maintenance. Am J Clin Nutr 47 : 19–25, 1988.

23.

Kraegen EW, Storlien LH, Jenkins AB, James DE. Chronic exercise compensates for insulin resistance induced by a high-fat diet in rats. Am J Physiol 256 : E242–E249, 1989.

24.

Bell RR, Spencer MJ, Sherriff JL. Voluntary exercise and monounsaturated canola oil reduce fat gain in mice fed diets high in fat. J Nutr 127 : 2006–2010, 1997.

25.

USDA. Counselor and Attache Reports. Official Statistics, USDA Estimates, USDA Foreign Agricultural Service, Oilseeds, and Products Division. Washington, DC: USDA, 1997.

26.

Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: Final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76A rodent diet. J Nutr 123 : 1939–1951, 1993.

27.

Trinder P. Determination of blood glucose using an oxidase-peroxidase system with a non-carcinogenic chromogen. J Clin Path 22 : 158–161, 1969.

28.

Bucolo G, David H. Quantitative determination of serum triglycerides by the use of enzymes. Clin Chem 19 : 476–482, 1973.

29.

Lo S, Russell JC, Taylor AW. Determination of glycogen in small tissue samples. J Appl Physiol 28 : 234–236, 1970.

30.

Folch JM, Lees M, Sloane-Stanley GH. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226 : 1861–1869, 1957.

31.

Jen K-LC, Greenwood MRC, Brasel JA. Sex differences in the effects of high-fat feeding on behavior and carcass composition. Physiol Behav 27 : 161–166, 1981.

32.

Deutsch DD, Jen KL-C, Grunberger G. Regulation of hepatic insulin receptor tyrosine kinase in rat models of mild insulin resistance. J Lab Clin Invest. 122 : 421–425, 1993.

33.

Legro RS, Finegood D, Dunaif A. A fasting glucose to insulin ratios is a useful measure of insulin sensitivity in women with polycystic ovary syndrome. J Clin Endocrinol Metab. 83 : 2694–2698, 1998.

34.

Gaiva MH, Couto RC, Oyama LM, Couto GE, Silveira VL, Riberio EB, Nascimento CM. Polyunsaturated fatty acid-rich diets: effect on adipose tissue metabolism in rats. Br J Nutr 86 : 371–377, 2001.

35.

Fickova M, Hubert P, Cremel G, Leray C. Dietary (n-3) and (n-6) polyunsaturated fatty acids rapidly modify fatty acid composition and insulin effects in rat adipocytes. J Nutr 128 : 512–519, 1998.

36.

Feskens EJ, Kromhout D. Habitual dietary intake and glucose tolerance in euglycemic men: The Zutphen Study. Int J Epidemiol 19 : 953–959, 1990.

37.

Cleary MP, Phillips FC, Morton RA. Genotype and diet effects in lean and obese Zucker rats fed either safflower or coconut oil diets. Proc Soc Exp Biol Med 220 : 153–161, 1999.

38.

Hill JO, Peters JC, Lin D, Yakubu F, Greene H, Swift L. Lipid accumulation and body fat distribution is influenced by type of dietary fat fed to rats. Int J Obes 17 : 223–226, 1993.

39.

Jen K-LC, Alexander M, Zhong S, Rose K, Lin PKH, Kasim SE. Lipid lowering effect of omega-3 fatty acids in genetically obese Zucker rats. Nutr Res 9 : 1217–1228, 1989.

40.

Feskens EJ, Bowles CH, Kromhout D. Inverse association between fish intake and risk of glucose intolerance in normoglycemic elderly men and women. Diabetes Care 14 : 935–941, 1991.

41.

Leyton J, Drury PJ, Crawford MA. Differential oxidation of saturated and unsaturated fatty acids in vivo in the rat. Br J Nutr 57 : 383–393, 1987.

42.

DeLany JP, Windhauser MM, Champague CM, Bray GA. Differential oxidation of individual dietary fatty acids in humans. Am J Clin Nutr 72 : 905–911, 2000.

43.

Storlein LH, Kriketos AD, Calvert GD, Baur LA, Jenkins AB. Fatty acids, triglycerides and syndromes of insulin resistance. Prostaglandins Leukot Essent Fatty Acids 57 : 379–385, 1997.

44.

Harris WS, Connor WE, McMurry MP. The comparative reductions of the plasma lipids and lipoproteins by dietary polyunsaturated fats: Salmon oil versus vegetable oils. Metabolism 32 : 179–184, 1983.

45.

Phillipson BE, Rothrock DW, Connor WE, Harris WS, Illingworth DR. Reduction of plasma lipids, lipoproteins, and apoproteins by dietary fish oils in patients with hypertriglyceridemia. N Eng J Med 312 : 1210–1219, 1985.

46.

Randle PJ, Kerbey AL, Espinal J. Mechanisms decreasing glucose oxidation in diabetes and starvation: role of lipid fuels and hormones. Diab Metab Rev 4 : 623–638, 1988.

47.

Wilkes JJ, Bonen A, Bell RC. A modified high-fat diet induces insulin resistance in rat skeletal muscle but not adipocytes. Am J Physiol 275 : E679–E686, 1998.

48.

Mingrone G, DeGaetano A, Greco AV, Capristo E, Benedetti G, Castagneto M. Reversibility of insulin resistance in obese diabetic patients: Role of plasma lipids. Diabetologia 40 : 599–605, 1997.

49.

Hickey MS, Houmard JA, Considine RV, Tyndall GL, Midgette JB, Gavigan KE, Weidner ML, McCammon MR, Israel RG, Caro JF. Gender-dependent effects of exercise training on serum leptin levels in humans. Am J Physiol 272 : E562–E566, 1997.