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(Journal of Nutrition. 2000;130:27-29.)
© 2000 The American Society for Nutritional Sciences

Research Communication

An Isomeric Mixture of Conjugated Linoleic Acids But Not Pure cis-9,trans-11-Octadecadienoic Acid Affects Body Weight Gain and Plasma Lipids in Hamsters1

Victor C. Gavino2, Grace Gavino, Marie-Josée Leblanc and Beatriz Tuchweber

Département de Nutrition, Faculté de Médecine, Université de Montréal, Montréal Qc, Canada H3C 3J7

2To whom correspondence should be addressed.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
We report the effect of an atherogenic diet supplemented with cis-9,trans-11-octadecadienoic acid (c9t11), linoleic acid (LA) or an isomeric mixture of conjugated linoleic acids (CLA) on plasma lipids, weight gain and food intake of male Golden Syrian hamsters. Animals were assigned to three diet groups (n = 10), and fed nonpurified diet, supplemented with 10% hydrogenated coconut oil and 0.05% cholesterol for 6 wk. The first diet group was further supplemented with 1% CLA (CLA group), the second diet group with 0.2% c9t11 (c9t11 group) and the third group with 0.2% LA (LA group). The diets were designed to have equivalent levels of c9t11 in the CLA and c9t11 groups. At 2 and 6 wk of feeding, the CLA group had significantly lower plasma triglyceride and total cholesterol concentrations than either the c9t11 or the LA groups. HDL-cholesterol did not differ among diet groups. The CLA group had significantly lower weight gain but greater food intake than either the c9t11 or the LA groups. There were no significant differences between the c9t11 and the LA groups in any of the variables measured. We conclude that under our experimental conditions of short-term feeding, c9t11, thought to be the active compound in CLA, does not produce the same effect as the isomer mixture.

KEY WORDS: • hamsters • conjugated linoleic acid • cholesterol • linoleic acid • cis-9,trans-11-octadecadienoic acid


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Conjugated linoleic acid (CLA),3 a generic term applied to a collection of positional and geometric isomers of linoleic acid (LA) with a conjugated double-bond system, has been reported to have beneficial effects on blood lipids and early signs of atherogenesis (Lee et al. 1994Citation , Nicolosi et al. 1997Citation ). Among the various isomers of CLA, cis-9,trans-11-octadecadienoic acid (c9t11) is assumed to be the bioactive agent because of its abundance in natural food products (Chin et al. 1992Citation , Ha et al. 1989Citation , Parodi 1997Citation , Sehat et al. 1998aCitation ). Furthermore, it appears to be concentrated in vivo (Sehat et al. 1998bCitation ). Analysis of CLA isomer mixtures with the latest techniques shows that commercial preparations contain up to 30% c9t11 (Christie et al. 1997Citation ). This figure may be the sum of a mixture of the cis-9,trans-11 and trans-9,cis-11 isomers (Sehat et al. 1998bCitation ). Synthesis of c9t11 in pure form has been described (Berdeaux et al. 1997Citation ) and it is now commercially available. Thus, we tested whether pure c9t11 has the same plasma lipid-lowering effects in hamsters as when it is given in equivalent amounts as a CLA isomer mixture.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Animals and diets.

The experimental protocol was reviewed and approved by the Animal Care Committee of the Université de Montréal in accordance with the guidelines of the Canadian Council on Animal Care. Male Golden Syrian hamsters (100–110 g) were obtained from Charles River Breeding Laboratories (St. Constant, Quebec Canada). They were distributed into three groups of 10, housed 5 per cage in plastic cages with wood chip bedding and kept at 20°C in a room with a 12 h dark-light cycle. After acclimation, we followed the dietary protocol previously described by others (Kowala et al. 1993Citation , Otto et al. 1995Citation ) to induce atherosclerosis in hamsters. They were given free access to a mild atherogenic diet consisting of Rodent Chow 5001 (Agribrands-Purina Canada, Strathroy ON Canada)4 supplemented with 10 g/100 g hydrogenated coconut oil (ICN, Mississauga, ON, Canada), and 0.05 g/100 g cholesterol (ICN). The fatty acid profile of this diet is shown in Table 1Citation . The three test diets fed to the three groups consisted of the mild atherogenic diet plus one of the following: CLA (Nu-Chek-Prep, Elysian, MN) at 10 g/kg diet (CLA group); c9t11 (Matreya, Pleasant Gap, PA) at 2 g/kg diet (c9t11 group); or LA (Nu-Chek-Prep) at 2 g/kg diet (LA group). The test diets were prepared fresh biweekly and stored at -20°C. Diets were replaced twice a week, and food disappearance was measured at the same time.


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  		Table 1. Fatty acid composition of the test diets

 
Analytical methods.

Blood was collected via the retro-orbital sinus of fed hamsters into EDTA blood collection tubes. Plasma was collected after centrifugation at 2,500 x g for 15 min. Plasma total cholesterol was measured using Sigma Diagnostics Cholesterol kit (Sigma, Oakville ON, Canada), while triglycerides were measured using a Peridochrom Triglycerides GPO-PAP kit (Boehringer Mannheim, Montreal QC, Canada). Both methods are colorimetric. After precipitation of apolipoprotein B (apoB)-containing lipoproteins with a phosphotungstate reagent (Boehringer Mannheim), HDL-cholesterol in the supernatant was assayed enzymatically as above.

Miscellaneous procedures.

Lipid content of the diet was determined by a Soxhlet procedure while protein was estimated by Kjeldahl (Kjeltec, Fisher Scientific, Ottawa, ON, Canada). Diet fatty acid composition of each batch was monitored by gas chromatography using a 30 m Carbowax capillary column (Chromatographic Specialties, Brockville, ON, Canada). Lipid extracts were prepared for gas chromatographic analysis by methylation of any unesterified fatty acids with diazomethane followed by transmethylation of fatty acid glycerol esters with NaOCH3 (Christie 1989Citation ).

Statistical analysis.

Body weights and weight gains were analyzed by repeated measures ANOVA using simple contrasts to compare diet groups (main effects). Food disappearance data were analyzed by two-way ANOVA using diet and day of measurement as the grouping factors. Blood lipid data at 2 and 6 wk were analyzed by one-way ANOVA using diet as the grouping factor. All post-hoc multiple comparisons were made using the Tukey HSD test. Significant difference was declared at P < 0.05. Statistical routines available in SPSS (SPSS Inc., Chicago IL) were used.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
The c9t11 and LA group diet fatty acid profiles were nearly identical except for 18:2, which was partially replaced by pure c9t11 in the c9t11 group (Table 1)Citation . The LA group therefore served as the control for the c9t11 group. The CLA group was designed to consume a similar amount of c9t11 as the c9t11 group to address the question of whether c9t11 alone exerts the same biological effects as when it is given in a mixture with other CLA isomers. Since commercial CLA preparations contain from 20 to 30% c9t11 (Christie et al. 1997Citation , Sehat et al. 1998bCitation ), we added 4-fold more CLA to the CLA group diet relative to the mass of c9t11 added to the c9t11 group diet. Table 1Citation reflects this difference.

The diets were well accepted over the feeding period. We used food disappearance data as an estimate of food intake. Food disappearance per hamster per day in the CLA group (13 ± 0.3 g) was significantly higher than either the c9t11 or the LA groups, both of which were 12.1 ± 0.3 g. (means ± SE, n = 12). The CLA group had significantly lower weight gain than either the c9t11 or LA groups which did not differ (Fig. 1Citation ).



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  		Figure 1. Effect of conjugated linoleic acid (CLA), cis-9,trans-11-octadecadienoic acid (c9t11) and linoleic acid (LA) on body weights and weight gains of hamsters. Points represent means of 10 animals ± SE. Panel A: body weight (g) from d 0 to d 43 of the feeding period. Panel B: weight gain from d 8 to d 43 relative to the original weight at d 1 of feeding. Data were analyzed by repeated measures ANOVA. An asterisk denotes significant difference from the other groups, P < 0.05, Tukey HSD. The entire weight gain curve for the CLA group was significantly lower than the c9t11 and LA groups, P < 0.05, simple contrast, main effects (Panel B).

 
Previous CLA-feeding studies on rodents have given different results, presumably depending on the experimental conditions used. Chin et al. (1994)Citation reported that 0.5% dietary CLA enhanced the growth rates of rat pups even though feed intake did not differ from controls. In experiments with ICR mice, the same group reported that 0.5% dietary CLA did not affect body weights of male mice and only slightly, but not significantly, decreased weight gain in female mice in parallel with a decrease in food intake (Park et al. 1997Citation , Park et al. 1999aCitation , Park et al. 1999bCitation ). In contrast, West et al. (1998)Citation found that 1% dietary CLA significantly reduced the growth rate of AKR/J mice regardless of the amount of fat in the feed, through mechanisms related to a reduction in energy intake and metabolic rate. In dose-response experiments, the same group showed that even when energy intake did not differ between groups, dietary CLA significantly reduced growth rate, principally by reducing body fat deposition (Delany et al. 1999Citation ). We followed the experimental protocol described by Nicolosi et al. (1997)Citation for hamsters except that we did not add safflower oil to the feed and used half the quantity of dietary cholesterol. In accordance with previous reports (Krause et al. 1992Citation , Nicolosi et al 1998Citation ), we used nonpurified diet instead of semipurified diet to induce a lipoprotein profile in hamsters associated with atherogenesis. In contrast to our results, Nicolosi et al. (1997)Citation reported that none of the levels of CLA in the diet, from 0.06 to 1.1% total energy, affected the body weights of the hamsters differently from the LA group. They did find, however, that both the CLA and LA groups had lower final body weights than the control group. At present, we do not have a mechanistic explanation for why differences in experimental conditions and different rodent species lead to different growth responses to dietary CLA. Preliminary results from body composition analysis indicate that under our experimental conditions, hamsters fed CLA accumulate less fat mass than those fed c9t11 or LA (unpublished observations), a factor that could have influenced body weight gain in the CLA group. We suggest that the net effect of CLA may depend in part on the specific proportions of the individual isomers in the CLA used because the different isomers may have different biological activities.

Similar to the results of Nicolosi et al. (1997)Citation , HDL-cholesterol was not affected by the diets at either time point (Table 2Citation ).In contrast, CLA, but not c9t11 alone, lowered plasma triglycerides and total cholesterol at 2 and 6 wk of feeding relative to LA. Blood from animals with free access to food has high levels of chylomicrons and VLDL, both of which contain triglycerides and cholesterol. Hamsters store food in their cheek pouches and thus they are in a sense eating continuously but at a rate impossible to quantify. Thus, it is not surprising that changes in blood triglyceride would be accompanied by parallel changes in blood cholesterol.


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  		Table 2. Effect of dietary conjugated linoleic acid (CLA), cis-9,trans-11-octadecadienoic acid (c9t11) and linoleic acid (LA) on plasma total triglycerides, total cholesterol, HDL-cholesterol and non-HDL-cholesterol of hamsters1

 
We cannot explain how CLA lowers weight gain in hamsters. One possibility may be through CLA-induced attenuation of fat absorption and transport after a meal. To test this possibility, we measured blood triglycerides in the hamsters that had free access to food. The results suggest that combined CLA isomers, but not pure c9t11 alone, can disrupt assimilation and/or transport of fat as lipoprotein triglyceride. The CLA-induced decrease in plasma triglycerides is consistent with the observed differences in weight gain curves (Fig. 1)Citation . It is unlikely that adipose lipoprotein lipase plays a role in CLA-induced plasma triglyceride reduction. Previous reports consistently showed that fat depots are reduced by dietary CLA (Delany et al. 1999Citation , Park et al. 1997Citation , Park et al. 1999aCitation , Park et al. 1999bCitation , West et al. 1998Citation ) and that CLA reduces lipoprotein lipase activity in 3T3-L1 adipocytes (Park et al. 1997Citation ).

Park et al. (1999b)Citation recently reported that CLA-induced body composition changes in mice are associated with the trans-10,cis-12 isomer and not c9t11. We suggest that the same may be true in hamsters. This could explain why the growth curves for the c9t11 and LA groups did not differ (Fig. 1)Citation . Park et al. (1999b)Citation found that the growth curve of mice fed with the highest concentrations of c9t11 (72.4% of total CLA) was the most similar to that of the control group.

In conclusion, dietary CLA under our experimental conditions slightly but significantly reduced weight gain in hamsters in spite of greater food consumption. This effect may be due to mechanisms involving dietary fat assimilation and lipid transport in blood. The c9t11 at amounts equivalent to that found in the CLA mixture did not have the same effects. The c9t11 may need to act synergistically with the other CLA isomers to exert its biological effects.


   FOOTNOTES
 
1 Supported in part by the Dairy Farmers of Canada. Back

3 Abbreviations used: apoB, apolipoprotein B; CLA, conjugated linoleic acid; LA, linoleic acid; c9t11, cis-9,trans-11-octadecadienoic acid. Back

4 Proximate composition: protein, 23.4%; fat, 4.5%; crude fiber, 5.8%; carbohyrates, 49%. Back

Manuscript received June 2, 1999. Revision accepted October 8, 1999.


   REFERENCES
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 

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2. Chin S. F., Liu W., Storkson J. M., Ha Y. L., Pariza M. W. Dietary sources of conjugated dienoic isomers of linoleic acid, a newly recognized class of anticarcinogens. J. Food Comp. Anal. 1992;5:185-197

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4. Christie W. W. Gas Chromatography and Lipids 1989:69-71 The Oily Press Ayr Scotland

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7. Ha Y. L., Grimm N. K., Pariza M. W. Newly recognized anticarcinogenic fatty acids: Identification and quantitation in natural and processed cheeses. J. Agric. Food Chem. 1989;37:75-81

8. Kowala M. C., Mazzucco C. E., Hartl K. S., Seiler S. M., Warr G. A., Abid S., Grove R. I. Prostacyclin agonists reduce early atherosclerosis in hyperlipidemic hamsters. Octimibate and BMY 42393 suppress monocyte chemotaxis, macrophage cholesteryl ester accumulation, scavenger receptor activity, and tumor necrosis factor production. Arterioscler. Thromb. 1993;13:435-444[Abstract/Free Full Text]

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12. Nicolosi R. J., Wilson T. A., Lawton C., Rogers E. J., Wiseman S. A., Tijburg L. B. M., Kritchevsky D. The greater atherogenicity of nonpurified diets versus semipurified diets in hamsters is mediated via differences in plasma lipoprotein cholesterol distribution, LDL oxidative susceptibility, and plasma alpha-tocopherol concentration. J. Nutr. Biochem. 1998;9:591-597

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15. Park Y., Albright K. J., Storkson J. M., Liu W., Cook M. E., Pariza M. W. Changes in body composition in mice during feeding and withdrawal of conjugated linoleic acid. Lipids 1999;34:243-248[Medline]

16. Park Y., Storkson J. M., Albright K. J., Liu W., Pariza M. W. Evidence that the trans-10,cis-12 isomer of conjugated linoleic acid induces body composition changes in mice. Lipids 1999;34:235-241[Medline]

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