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Articles

Reduced Hepatic Triglyceride Secretion in Rats Fed Docosahexaenoic Acid–Rich Fish Oil Suppresses Postprandial Hypertriglyceridemia

Ikuo Ikeda^*1, Jun Kumamaru^*, Noriaki Nakatani^*, Masanobu Sakono, Itsuki Murota^* and Katsumi Imaizumi^*

^* Laboratory of Nutrition Chemistry, Department of Bioscience and Biotechnology, Faculty of Agriculture, Graduate School Kyushu University, Fukuoka, 812-8581 Japan and Laboratory of Food Science and Nutrition, Department of Biochemistry and Applied Biosciences, Faculty of Agriculture, Miyazaki University, Miyazaki, 889-2192 Japan

¹To whom correspondence should be addressed. E-mail: iikeda{at}agr.kyushu-u.ac.jp

	ABSTRACT

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To evaluate the mechanisms of suppression of postprandial hypertriglyceridemia by fish oil rich in docosahexaenoic acid, the effect on the intestinal absorption of triglyceride, activities of lipoprotein lipase (LPL) and hepatic triglyceride lipase (HTGL) and metabolism of chylomicrons (CM) and CM remnants were compared with that of safflower oil in Sprague-Dawley rats in a series of studies. The feeding of fish oil for 3 wk suppressed postprandial hypertriglyceridemia (study 1). Dietary fish oil did not alter the rate of lymphatic absorption of triglyceride (study 2). The activities of LPL and HTGL were measured at 5 h after the beginning of feeding, when serum triglyceride concentrations were highest in both dietary groups. The activities of LPL in adipose tissue and heart were greater (P < 0.05) and those of HTGL were lower (P < 0.05) in the rats fed fish oil (study 3). In contrast, there were no differences in the activities of LPL and HTGL in postheparin plasma between the fish and safflower oil groups (study 4). The clearance rates of CM and CM remnants were measured by injecting intravenously CM collected from rats fed safflower or fish oils with [¹⁴C]triolein and [³H]cholesterol (study 5). Dietary oil did not influence the half-lives of CM or CM remnants. The secretion of triglyceride from the liver of rats injected with Triton WR-1339 was lower (P < 0.05) in the rats fed docosahexaenoic acid, a major component of fish oil, than those fed linoleic acid, a major component of safflower oil (study 6). These observations strongly support the hypothesis that in rats, the principal cause of the suppression of postprandial hypertriglyceridemia by fish oil is the depression of triglyceride secretion from the liver.

KEY WORDS: • chylomicrons • docosahexaenoic acid • fish oil • lipoprotein lipase • rats

	INTRODUCTION

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Recent studies have shown that postprandial hypertriglyceridemia may be associated with the risk of coronary heart disease (1 2 3) . It has been established that the feeding of fish oil suppresses plasma triglyceride concentrations in both postprandial and fasting states in humans and experimental animals (1 ,4) . Although the reduction in plasma triglyceride concentration in the fasting state is ascribed to the suppression of hepatic fatty acid and triglyceride synthesis (5 6 7 8) , the reason why dietary fish oil suppresses postprandial hypertriglyceridemia has not been determined (1 ,4) . There have been several conflicting observations on this phenomenon. Because several metabolic events that occur after the digestion and absorption of dietary fats are correlated with one another and determine postprandial triglyceride concentration in plasma, the entire spectrum of metabolic events should be evaluated. However, most studies have examined only some of the metabolic effects of dietary fish oil.

The effect of fish oil on triglyceride concentrations in postprandial plasma has been ascribed to the constituent (n-3) polyunsaturated fatty acids (PUFA).² Because most fish oils contain more eicosapentaenoic acid (EPA) than docosahexaenoic acid (DHA), it was thought that EPA contributes to the suppression of postprandial hypertriglyceridemia (1) . However, a few studies showed that DHA was also effective in reducing plasma triglyceride concentration after a meal (9 ,10) . Almost all of these studies were conducted in humans. To elucidate more detailed mechanisms of the suppression of postprandial hypertriglyceridemia by dietary fish oil, it seems essential to use animal models.

In the present study, using rats, we examined the effect of fish oil rich in DHA on the absorption of triglycerides, activities of lipoprotein lipase (LPL) and hepatic triglyceride lipase (HTGL), the metabolism of chylomicrons (CM) and CM remnants and the secretion of triglycerides from the liver.

	MATERIALS AND METHODS

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Diet.

DHA-rich fish oil was kindly provided by Sagami Chemical Research Center (Kanagawa, Japan). High linoleic and high oleic safflower oils and palm oils were supplied by Rinoru Oil Mills (Tokyo, Japan) and Fuji Oil (Tokyo, Japan), respectively. Fish and high linoleic safflower oils were used as the dietary fat sources in studies 1–5. Fish oil was supplemented with 10% of high linoleic safflower oil to avoid linoleic acid (LA) deficiency. In study 6, ethyl esters of DHA and EPA were used as sources of dietary (n-3) PUFA. (n-3) PUFA were added at 10% dietary fat. Other fatty acids were adjusted to the same composition by mixing palm and high oleic and high linoleic safflower oils in study 6. Dietary fats in the LA group contained LA instead of (n-3) PUFA. The fatty acid compositions of the dietary fats are shown in Table 1 . The experimental diets were prepared according to the recommendation of the American Institute of Nutrition (AIN) (11) and contained 200 g casein, 100 g fat, 10 g vitamin mixture (AIN-76), 35 g mineral mixture (AIN-76), 2 g choline bitartrate, 3 g dl-methionine, 50 g cellulose, 150 g corn starch and up to 1000 g sucrose per 100 g diet. Vitamin and mineral mixtures were purchased from Nihon Nosan Kogyo (Tokyo, Japan).

Male Sprague-Dawley rats (SPF, 5 wk old; Seac Yoshitomi, Fukuoka, Japan) were kept in an air-conditioned room (22–23 °C, lights on 0800–2000 h). These rats were meal-fed a purified diet containing fish or high linoleic safflower oils for 2 h (from 1000 to 1200 h) for 3 wk. On the last day, after blood samples were taken from the tail vein (0 time), rats were meal-fed 10 g of a diet for 1 h. They consumed all of the food within 1 h. Blood was collected from the tail vein at 1, 3, 5 and 7 h after the beginning of the feeding. Serum was obtained through centrifugation.

Study 2: effect of dietary fish and safflower oils on lymphatic recovery of [¹⁴C]triolein in rats cannulated thoracic duct.

Male Sprague-Dawley rats (5 wk old) consumed ad libitum the same diets as in study 1 for 3 wk. The left thoracic lymphatic duct cephalad to the cisterna chyle was cannulated with the use of pentobarbital (Nembutal) anesthesia as described previously (12 13 14) . A second indwelling catheter was placed in the stomach for the administration of a test emulsion. After surgery, the rats were placed in restraining cages and intragastrically administered a continuous infusion of a solution containing 139 mmol glucose and 85 mmol NaCl per L at a rate of 3.4 mL/h until the end of the experiment. The same solution was given as drinking water. On the next morning, rats with a constant lymph flow rate were administered an emulsion containing glycerol tri-[1-¹⁴C]oleate ([¹⁴C]triolein, 1.58 GBq/mmol; Amersham Pharmacia Biotech, Buckinghamshire, U.K.). The test emulsion contained 200 mg sodium taurocholate (Nacalai Tesque, Kyoto, Japan), 50 mg fatty acid–free bovine albumin fraction V (BSA; Bayer Corp.), 200 mg triolein (Sigma Aldrich Japan, Tokyo, Japan) and 37 kBq [¹⁴C]triolein. Lymph was collected in ice-chilled tubes containing EDTA, and the radioactivity was measured with a liquid scintillation counter.

Study 3: effect of dietary fish and safflower oils on activities of LPL in adipose tissue and heart and of HTGL.

The feeding conditions of male Sprague-Dawley rats (5 wk old) were the same as in study 1. In study 1, the serum triglyceride concentration was highest at 5 h after feeding in both dietary groups (Fig. 1 ). Therefore, rats were killed at 5 h after a meal was offered. Liver, heart and perirenal adipose tissue were excised, frozen in liquid nitrogen and kept at -80°C until analyzed.

View larger version (19K): [in this window] [in a new window]   Figure 1. Postprandial hypertriglyceridemia in rats meal-fed a diet containing fish or safflower oil for 3 wk and then offered 10 g of the same diet for 1 h (study 1). After the collection of blood from the tail vein (time 0), rats were fed a meal of 10 g of a diet for 1 h and blood was collected at 1, 3, 5 and 7 h after the beginning of the feeding. As described in Results, the concentrations of serum triglycerides at time 0 differed between the fish oil and the safflower oil groups. Therefore, serum triglyceride concentrations at time 0 were subtracted from those after meal feeding. Data are means ± SE, n = 6. *P < 0.05 and **P < 0.01, significantly different from the safflower oil group.

The feeding conditions of male Sprague-Dawley rats (5 wk old) were the same as in study 1. At 5 h after a meal was offered, heparin (100 U/100 g body) was injected into the tail vein (15) . After 5 min, aortic blood was collected, and postheparin plasma was obtained through centrifugation.

Study 5: effect of dietary fish and safflower oils on metabolism of CM and CM remnants.

Male Sprague-Dawley rats (5 wk old) consumed ad libitum the same diets as in study 1 for 3 wk. Rats from each group were separated into donors and recipients. The thoracic duct of the donor rats was cannulated as described earlier, and on the next morning, an emulsion containing 200 mg fish or safflower oil plus 1.11 MBq [¹⁴C]triolein and 9.25 MBq [1,2(n)-³H]cholesterol (1.50 TBq/mmol; Amersham Pharmacia Biotech) was administered via a stomach tube. Up to 15 mL of lymph, which became turbid and white 30 min after administration, was collected for 6 h in a tube containing 150 µL of a solution of 270 mmol EDTA/L, 10 mmol ascorbic acid/L and 1.5 mg gentamicin sulfate (16) . Lymph was kept at room temperature until CM separation. On the next morning, lymph was ultracentrifuged at 36,000 x g for 40 min at 20 °C, and the CM layer was aspirated. Recipient rats were anesthetized with diethyl ether; a PE-50 tube was inserted into the aorta via the left carotid artery, and a second tube was inserted into the right superior vena cava via the right jugular vein (17) . In the afternoon, CM (500 µL) were injected into the right superior vena cava, and a 400-µL blood sample was taken periodically from the aorta via an inserted tube. After the blood sampling, 400 µL of saline was injected. Serum was separated through centrifugation, and the radioactivity was measured with a liquid scintillation counter.

Study 6: effect of dietary LA, EPA or DHA on the secretion rate of triglycerides from the liver.

Male Sprague-Dawley rats (5 wk old) consumed ad libitum a diet containing LA, EPA or DHA for 3 wk. At the end of the study, after 7 h of food deprivation, blood was taken from the tail vein, and Triton WR-1339 (600 mg/kg body) was administered via the tail vain (15) . Blood samples were taken at 120 and 240 min after Triton WR-1339 administration.

Rats in these studies were killed by aortic blood withdrawal while under diethyl ether anesthesia. All animal studies were carried out under the guidelines for animal experiments of the Faculty of Agriculture, Graduate School Kyushu University (Fukuoka, Japan) and Law 105 and Notification 6 of the government of Japan.

Biochemical analyses.

Serum triglycerides were enzymatically assayed with a commercial kit (Triglyceride G Test; Wako Pure Chemicals, Osaka, Japan).

Activities.

The activity of LPL was analyzed in perirenal adipose tissue and heart. After the preparation of acetone powder, the activity was measured by using [¹⁴C]triolein as a substrate (18 ,19) . For the measurement of HTGL activity (20 ,21) , after homogenization of the liver with 4 mL of ice-cold 100 mmol phosphate/L buffer, pH 7.4, containing 5 x 10³ U heparin/L, the homogenate was centrifuged at 2000 x g for 20 min at 0°C. The supernatant was used as the enzyme source. [¹⁴C]Triolein was used as a substrate. To measure the activities of LPL and HTGL in postheparin plasma, the plasma was used as the enzyme source and safflower and fish oils were used as substrates. Protein was measured according to the method of Lowry et al. (22) using bovine serum albumin as a standard.

Statistical analysis.

All values are expressed as means ± SE. Data were analyzed by ANOVA, followed by Student’s t test or Duncan’s new multiple range test (23) . Differences were considered significant at P < 0.05.

	RESULTS

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There were no differences in food intake and growth indices between the fish and safflower oil groups in studies 1–5 or among the LA, EPA and DHA groups in study 6 (data not shown).

Study 1.

The concentration of serum triglycerides at time 0 was significantly lower in the fish oil group than in the safflower oil group (0.545 ± 0.132 and 0.922 ± 0.298 mmol/L, respectively). This can be due to the suppression of hepatic fatty acid and triglyceride synthesis by fish oil (5 6 7 8) . The serum triglyceride concentration at time 0 was subtracted from those after a meal. Increases in serum triglycerides (after subtraction) at several possible time points are shown in Fig. 1 . The serum triglyceride concentration was significantly higher in the safflower oil group than in the fish oil group at 5 and 7 h after a meal. The area under the curve (AUC) of serum triglyceride was 7.47 ± 1.41 and 4.54 ± 0.84 mmol/L x h in the safflower and fish oil groups, respectively.

The serum cholesterol concentration at time 0 was significantly lower in the fish oil group than in the safflower oil group. No significant difference was found between rats fed safflower and fish oils after a meal (data not shown).

Study 2.

There were no differences in periodic and total 24-h recoveries of triolein in lymph between rats that had been fed safflower and fish oils. The total 24-h recoveries of triolein were 86.0 ± 2.4 and 84.9 ± 3.6% in rats fed safflower and fish oils, respectively.

Study 3.

The activities of LPL and HTGL were measured at 5 h after the beginning of meal-feeding in studies 3 and 4. The activity of LPL in adipose tissue and heart was significantly higher in the fish oil group than in the safflower oil group (Fig. 2 ). In contrast, HTGL activity was significantly lower in the fish oil group.

View larger version (42K): [in this window] [in a new window]   Figure 2. The activities of lipoprotein lipase (LPL) in adipose tissue and heart and of hepatic triglyceride lipase (HTGL) in rats meal-fed a diet containing fish or safflower (Saf) oil for 3 wk and then offered 10 g of the same diet for 1 h (study 3). On the last day, 5 h after the meal, rats were killed, and adipose tissue, heart and liver were excised. Data are means ± SE, n = 6. *P < 0.05, significantly different from the safflower oil group.

In rats fed safflower and fish oils, the activities of LPL were 181 ± 19 and 202 ± 13 nmol oleic acid released/(min · mg protein) and the activities of HTGL were 220 ± 16 and 256 ± 40 nmol oleic acid released/(min · mg protein), respectively. There were no differences in these enzyme activities between the two groups. When safflower or fish oils used as dietary fats were utilized as enzyme substrates, their hydrolysis rates by LPL and HTGL were also the same for postheparin plasmas obtained from rats fed safflower or fish oils (data not shown).

Study 5.

CM collected from donor rats fed diets containing safflower or fish oil were injected intravenously into recipient rats fed the same diets. Clearance rates of CM and CM remnants were estimated with [¹⁴C]triolein and [³H]cholesterol administered simultaneously with safflower or fish oil to donor rats, respectively. As shown in Fig. 3 , both CM and CM remnants disappeared linearly from the bloodstream in a semilogarithmic plot. The half-lives of CM were 5.1 ± 0.3 and 5.2 ± 0.2 min and those of the CM remnant were 8.1 ± 0.6 and 7.9 ± 0.4 min in the safflower and fish oil groups, respectively. These half-lives did not differ between the safflower and fish oil groups.

View larger version (28K): [in this window] [in a new window]   Figure 3. Metabolism of chylomicrons (CM) and CM remnants in rats consuming ad libitum a diet containing fish or safflower oil for 3 wk (study 5). Rats from each group were separated into donors and recipients. The thoracic ducts of the donor rats were cannulated, and the rats were fed their respective dietary fat with [14C]triolein and [3H]cholesterol. Lymph was collected, and CM were separated from the lymph. Recipient rats were injected with CM collected from rats fed their respective dietary fats in the superior vena cava, and aortic blood was collected periodically. Half-lives (t1/2) did not differ between groups. Data are means ± SE, n = 6.

Serum triglyceride concentrations before the injection of Triton WR-1339 (time 0) were significantly lower in the EPA and DHA groups than in the LA group (Fig. 4A ). Serum triglyceride concentrations linearly increased after the Triton WR-1339 injection. The rates of serum triglyceride secretion from the liver calculated at 0–120 min were significantly lower in the EPA and DHA groups than in the LA group (Fig. 4B ).

View larger version (20K): [in this window] [in a new window]   Figure 4. The secretion rate of triglycerides from the liver in rats consuming ad libitum diets containing linoleic acid (LA), eicosapentaenoic acid (EPA) or docosahexaenoic acid (DHA) for 3 wk (study 6). In the last day, after 7 h of food deprivation, blood was collected from tail vein, and Triton WR-1339 was then injected via the tail vein. Blood was collected at 120 and 240 min after administration. A, Periodic increases in serum triglyceride concentration. B, Secretion rate of triglycerides from the liver calculated between 0 and 120 min in A. Data are means ± SE, n = 6. Different superscript letters (at each time point in A) indicate significant difference, P < 0.05.

	DISCUSSION

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Lymphatic absorption of oleic acid given as triolein was the same when rats were fed a diet containing fish or safflower oil as the background diet (study 2). The results suggest that the long-term feeding of fish and safflower oils does not influence the processing rate of triglycerides from digestion in the intestinal lumen to the synthesis and secretion of CM in intestinal cells. Harris et al. (24) showed that when rats that were fed EPA and DHA in the background diet and had CM clearance blocked by Triton WR-1339 injection were gavaged with triolein, these (n-3) PUFA did not influence CM input to the bloodstream. Our experiments confirmed their observation. We and others previously showed that when relatively large amounts of fish oil or triglycerides containing EPA and DHA were gavaged to rats, the absorption of (n-3) PUFA was slower and less effective than that for vegetable oils and triolein (13 ,14 ,25) . This was ascribed to the slower hydrolysis by pancreatic lipase of EPA and DHA contained in fish oil triglycerides bound at the sn-1 and -3 positions of glycerol (14 ,26) . This event may influence the postprandial plasma triglyceride concentration. However, a study in humans showed that an increase in plasma triglycerides after fish oil feeding was the same as that after olive oil feeding (27) . We contend that when fish oil is taken in a physiological amount along with other foods, the influence on postprandial plasma triglyceride is the same as for vegetable oils.

CM secreted in lymph enter the bloodstream and are transported to peripheral tissues. CM triglycerides are hydrolyzed by LPL, which is present on the surface of capillaries in peripheral tissues with a high fatty acid requirement (1) . LPL is thought to be the rate-limiting enzyme in determining the rate of triglyceride clearance from plasma (1) . There are conflicting observations on the effect of dietary fish oil on LPL activity. Although some studies did not find any influence of dietary fish oil on postheparin LPL activity in humans (28 ,29) , others showed that fish oil feeding increased the activity of postheparin LPL (30) and endogenous non–heparin-stimulated LPL (31) . Controversial observations were also reported in studies in rats (8 ,20 ,32) . Benhizia et al. (20) and we (8) observed increases in LPL activity of adipose tissue due to the feeding of fish oil. In contrast, Haug and Hostmark (32) reported a reduction in the LPL activity in rats. LPL activities in various tissues are influenced by plasma insulin levels (1) . Several investigations have reported diverse effects of fish oil on plasma insulin levels and insulin sensitivity in experimental animals and humans (33 34 35 36) . However, because results obtained in these investigations are not necessarily consistent, the effect of fish oil in the regulation of LPL activity through plasma insulin level remains obscure.

Adipose tissue LPL is activated by insulin, which is secreted into the bloodstream after a meal. Therefore, we killed rats after the meal, when plasma triglyceride concentrations were highest. Although LPL activities in adipose tissue and heart were significantly higher in the rats fed the fish oil diet, the activity in postheparin plasma was not significantly influenced by the fish oil feeding (studies 3 and 4). It is not apparent which activity of LPL is reflected by the rate of CM triglyceride clearance. Because neither of the activities necessarily shows the actual physiological activity of LPL in vivo as suggested by Roche and Gibney (1) , direct measurement of the clearance rates of CM and CM remnants is essential.

In study 5, CM collected after the administration of safflower and fish oils in donor rats fed a diet containing one of these oils was intravenously injected into recipient rats fed the same diets. The clearance rates of CM and CM remnants were estimated with [¹⁴C]triolein and [³H]cholesterol administered simultaneously with safflower or fish oil to donor rats. The rates of the overall metabolism of CM and CM remnants were not influenced by the feeding of fish and safflower oils. Therefore, the activities of LPL in postheparin plasma, but not in adipose tissue and heart, were associated with the clearance rates of CM and CM remnants. Our observation is consistent with the study by Harris and Muzio (37) , in which plasma removal rate of CM like lipid emulsion was not altered by the feeding of fish oil in humans. Therefore, it seems that long-term feeding of fish oil does not accelerate the removal of triglycerides from the bloodstream. However, Harris et al. (24) observed an accelerated clearance of CM in rats fed fish oil compared with those fed oleic acid–rich oil. In their experiment, rats fed fish or oleic acid–rich oil as the background diet were fed soybean oil and their intestinal lymph was collected. The collected lymph was injected intravenously into rats fed fish or oleic acid–rich oil. The clearance rate of CM is influenced by many factors, such as the activities of LPL and HTGL and the concentrations of glucose, insulin and triglycerides. Therefore, there is a possibility that the clearance rate may change considerably with different experimental conditions. More accurate studies under the conditions in which CM metabolism is activated are necessary.

Lottenberg et al. (38) observed that the secretion of VLDL from the liver in rats that had been injected with Triton WR-1339 is suppressed by the feeding of fish oil containing EPA and DHA in similar amounts. Our results confirmed their observations and showed that EPA and DHA suppressed the secretion of triglycerides from the liver to the same extent (study 6). This observation strongly suggests that the major cause of the suppression of postprandial hypertriglyceridemia by fish oil is the reduction in triglyceride secretion from the liver, because the absorption of dietary fat and the clearance rates of CM and CM remnants were not influenced by dietary fish oil in our experiments.

We and others showed that dietary EPA and DHA suppressed the activity of enzymes related to fatty acid synthesis and suggested that the reduced synthesis of fatty acid in the liver decreased the secretion of triglycerides into the bloodstream (5 6 7) . In a human study, Harris et al. (39) demonstrated that dietary fish oil inhibited endogenous VLDL synthesis and secretion in the liver. However, several studies demonstrated that long-term feeding of fish oil reduced postprandial triglyceride concentrations in both CM and VLDL (24 ,37) . Because only VLDL are secreted from the liver, the reduction in CM triglycerides cannot be explained by the reduction in VLDL secretion. Roche and Gibney (1) suggested that low VLDL secretion by fish oil feeding may allow efficient clearance of CM triglycerides, because CM and VLDL compete for LPL. However, an enhanced clearance of CM was not observed in our experiments. Again, the clearance rates of CM and CM remnants should be accurately measured under conditions in which CM metabolism is activated. The establishment of this hypothesis can be a key to reveal the precise mechanisms of the suppression of postprandial hypertriglyceridemia by fish oil.

	FOOTNOTES

 
² Abbreviations used: AUC, area under the curve; CM, chylomicron(s); DHA, docosahexaenoic acid; EPA, eicosapentaenoic acid; HTGL, hepatic triglyceride lipase; LA, linoleic acid; LPL, lipoprotein lipase; PUFA, polyunsaturated fatty acids.

Manuscript received October 23, 2000. Initial review completed November 15, 2000. Revision accepted January 3, 2001.

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