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Experimental Biology and Medicine 228:843-849 (2003)
© 2003 Society for Experimental Biology and Medicine

ORIGINAL RESEARCH ARTICLE

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

K-L. Catherine Jen1, Anne Buison, Michael Pellizzon, Frank Ordiz, Jr., Lardo Santa Ana and Jordana Brown

Department of Nutrition and Food Science, Wayne State University, Detroit, Michigan 48202


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
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.

Key Words: high-fat diets • soybean oil • fish oil • palm oil • exercise • insulin sensitivity


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
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
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
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 IGo. The final four exercised and four sedentary groups were: CONEX, CONSD, FOEX, FOSD, POEX, POSD, SOEX, and SOSD.


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  		Table I. Diet Composition of Four Diets Used in This Study (g/kg)
 
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
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
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 IIGo). There was no difference among the four diet groups in blood glucose, insulin, and TG levels.


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  		Table II. Baseline Body Weight and Blood Parameters Before the Commencement of Exercise
 
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 IIIGo).


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  		Table III. Body Weight and Composition of Rats at Sacrifice
 
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 IIIGo), 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 IVGo). 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.


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  		Table IV. Blood Parameters of all Four Diet Groups as Well as Exercise and Nonexercise Subgroups of Rats at Sacrifice
 
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 VGo). 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.


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  		Table V. Liver Glycogen and Lipid Content of Four Diet Groups as Well as Exercise and Nonexercise Subgroups of Rats at Sacrifice
 
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 IIIGo). 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 IVGo 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 VGo).


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
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.


   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: cjen{at}sun.science.wayne.edu Back


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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Received for publication January 24, 2003. Accepted for publication February 27, 2003.





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