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Supplement: The WALTHAM International Sciences Symposia Innovations in Companion Animal Nutrition: Obesity and Weight Management

Postprandial Lipolytic Activities, Lipids, and Carbohydrate Metabolism Are Altered in Dogs Fed Diacylglycerol Meals Containing High- and Low-Glycemic-Index Starches^1–3,

John E. Bauer^*,4, Daisuke Nagaoka^*, Brandy Porterpan^*, Karen Bigley^*, Tomoshige Umeda and Katsuya Otsuji

^* Comparative Animal Nutrition Laboratory, Department of Small Animal Clinical Sciences, College of Veterinary Medicine and Faculty of Nutrition, Texas A&M University, College Station, TX, USA and Kao Corporation, Tokyo, Japan

⁴ To whom correspondence should be addressed. E-mail: jbauer{at}cvm.tamu.edu.

KEY WORDS: • diacylglycerol • glycemic index • postprandial • insulin • lipids • dogs

Digestion and assimilation of dietary fatty acids is a complex postprandial process involving triacylglycerol (TAG)⁵ hydrolysis, fatty acid absorption, resynthesis of TAG in intestinal mucosal cells, and chylomicron secretion. Dietary vegetable oils contain tri-, di-, and monoacylglycerols, although most edible oils contain approximately 87–98% of their acylglycerols as TAG, whereas diacylglycerols (DAG) comprise 0.8–9.5%. DAG is a glycerol with 2 acyl groups esterified to sn-1 and sn-2 (1,2-DAG) or sn-1 and sn-3 (1,3-DAG) positions (1). Canola oil contains 0.8% DAG, corn oil 2.8%, olive oil 5.5%, and cottonseed oil 9.5%. Oils enriched in DAG have recently become available and have recently been studied in several species. These oils contain >80% DAG of which 70% is 1,3-DAG, <20% TAG, <3% monoacylglycerol (MAG), and small amounts of antioxidants. Both 1,2-DAG and MAG are digestive intermediates of TAG, which are transiently generated in intestinal mucosal cells of the digestive tract.

Emulsions containing either DAG- or TAG-enriched oils were administered to rats, resulting in smaller TAG postprandial concentrations (2). Rats fed DAG-containing diets for 4 wk showed less weight gain than those on a TAG diet (3). In humans, weight reduction was observed when DAG replaced a part of dietary fat (4). Various mechanisms for potential antiobesity effects of DAG have been proposed (5,6). Cellular utilization of the 1,3-DAG results in different metabolic effects compared with TAG, and studies to date support the hypothesis that DAG oil increases fat oxidation in the liver or small intestine, thus limiting dietary fatty acid conversion to adipose tissue triglyceride. This effect may play a role in long-term weight management or reduction (4–7).

Little information is available on the effect of DAG-enriched oils on canine lipid metabolism. The present study was undertaken to provide comparative information in dogs regarding the postprandial effects of meals enriched in DAG vs. TAG oil on lipid, lipase, and carbohydrate metabolism. In addition, carbohydrate type was investigated by incorporating high- or low-glycemic-index carbohydrates in test meals used.

	MATERIALS AND METHODS

TOP MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Normal adult, intact female beagles ranging in age from 3 to 7 y (average 5.4 y) and body weights from 8.3 to 12.0 kg (average 10.9 kg) were used. Dogs were maintained according to protocols approved by the Texas A&M University Animal Care Committee. The dogs were fed meals containing vegetable oils enriched in either DAG or TAG. Two carbohydrates with different glycemic indices (GI) were also evaluated. Four meals were prepared using boiled boneless chicken breast (60 g) plus DAG or TAG (20 g) and either high-GI (HGI, gelatinized waxy corn starch) or low-GI (LGI, gelatinized high amylose corn starch) (25 g) carbohydrate. The meals were designated DAG/LGI, DAG/HGI, TAG/LGI, and TAG/HGI. A 4 x 4 Latin square design with 2-week washout periods between meals was used in which dogs were fed an extruded dry complete and balanced maintenance dog food. The DAG was supplied as Econa brand oil (Kao Corporation), and the TAG was a blend of commercially available vegetable oils (Kao Corporation). Both oils have been shown to have similar fatty acid compositions, caloric densities, and fatty acid weight fractions per gram (8). The starches were supplied by Nihon Shokuhin Kako Co., Ltd. Meals were calculated to contain approximately 366 kcal. Each meal accounted for approximately 50% of each dog's daily energy requirement and was readily consumed, providing discrete start-points for sampling. Blood was collected via jugular catheter into glass tubes containing EDTA, and plasma was immediately harvested at 0, 0.5, 1, 2, 3, 4, and 6 h after meal consumption. Aprotinin was added to aliquots of plasma to be used for insulin assay. TG, nonesterified fatty acids (NEFA), ß-hydroxybutyrate (ßHB), and glucose concentrations were also determined. Samples were stored frozen at –20°C until the time of analysis. At 6 h, postheparin plasma was collected 15 min after intravenous injection of 100 IU Na heparin/kg body wt. Lipoprotein lipase (LPL) and hepatic lipase (HL) of postheparin plasma were assayed using radiolabeled substrates (9).

Statistical analysis

Data are expressed as means + SEM. The effects of diet and time on postprandial plasma changes were evaluated via repeated-measures ANOVA, and significance was set at P < 0.05 or as noted. Where appropriate, multiple comparisons for main effects of diet, time, and diet x time interactions were performed at P < 0.05 (Statistix 7.0; Analytical Software). Where there was a significant interaction of group and time, contrasts were made using 1-way ANOVA followed by LSD tests to determine where the difference occurred. An experiment-wide type I error of 0.05 was maintained. All data were found to follow a normal distribution at P < 0.05 using the Shapiro-Wilk test. If variances were nonhomogeneous, log₁₀ transformed data were analyzed.

	RESULTS

TOP MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Main time effects were seen with all postprandial plasma data analyzed (P <0.001). Time x diet effects included decreased peak and duration of postprandial hypertriglyceridemia in dogs fed the DAG/HGI and DAG/LGI meals compared with the TAG meals at hours 2 and 3. This finding was independent of starch type (Fig. 1). Carbohydrate effects included higher plasma NEFA concentrations at hours 2, 3, and 4 with LGI-carbohydrate-containing meals (Fig. 1). With all meals a transient decrease of ß-hydroxybutyrate (ßHB) occurred at 1 h and then returned to premeal values. However, differences in plasma ßHB related to oil or starch type were not seen (Fig. 1) .

View larger version (17K): [in this window] [in a new window]   FIGURE 1  Postprandial response of plasma lipid-related metabolites of dogs fed various acylglycerol/glycemic index meals. Values are means + SEM, n = 12/group. Letters not in common for a time point are significantly different, P < 0.05.

View larger version (21K): [in this window] [in a new window]   FIGURE 2  Postprandial response of plasma carbohydrate metabolites of dogs fed various acylglycerol/glycemic index meals. Values are means + SEM, n = 12/group. Letters not in common for a time point are significantly different, P < 0.05.

View larger version (27K): [in this window] [in a new window]   FIGURE 3  Hepatic and lipoprotein lipase (LP lipase) activities of dogs 6 h after consuming various acylglycerol/glycemic index meals. Values are means + SEM, n = 12/group. Letters not in common for an enzyme activity tended to differ, P < 0.085.

	DISCUSSION

TOP MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Marked differences in insulin response found after feeding the HGI starch meal were not unexpected. No modification of this response was observed with dietary oil type. Thus, starch type has a dramatic effect on insulin responsiveness to meal feeding, whether or not DAG or TAG is present. It is noteworthy, however, that no differences in plasma glucose concentration were seen in any group other than the expected postprandial effect. Elevated circulating insulin concentrations would be expected to increase cellular glucose uptake. This finding suggests that more glucose was being made available from either glycogen or, more likely, other sources to maintain steady plasma concentrations.

The significant elevation of plasma NEFA with the LGI meals is also of interest. If glucose flux into cells had been decreased in the LGI groups as a result of an attenuated insulin response, then relatively more tissue lipolysis from storage sites would be favored, resulting in fatty acid mobilization and the NEFA elevations observed. It is well known that decreased insulin levels promote hormone-sensitive lipase activity and lipolysis (11). A less potent release of insulin with LGI starch might also result in less active utilization of circulating NEFA. Alternatively, increased intravascular lipolysis in response to the relative high fat content of the test meals may have occurred also, resulting in higher plasma NEFA. Taken together, these findings would favor adipogenesis overall with HGI starch compared with LGI starch resulting in greater risk of obesity. Data in rats have suggested that digestion and absorption of a LGI starch may be slower than HGI starch, leading to reduced lipogensis in adipose and liver tissues (12), whereas the apparent digestibility of LGI starch is similar to that of normal cornstarch (13). Canine studies have yet to be done on these particular questions.

Finally, HL and LPL activities were not different among the groups, although a tendency for higher HL values was seen when LGI starch was fed. It is unknown what effect diets containing DAG oil or LGI vs. HGI starches might have when fed for longer periods. Increased HL activities after feeding such diets, should they occur, would be consistent with increased HL-mediated high-density lipoprotein-bound TG lipolysis or cholesteryl ester uptake by the liver and also promote postprandial plasma triglyceride lowering (14). It is unknown at this time whether this may occur.

	FOOTNOTES

 
¹ Published in a supplement to The Journal of Nutrition. Presented as part of The WALTHAM International Nutritional Sciences Symposium: Innovations in Companion Animal Nutrition held in Washington, DC, September 15–18, 2005. This conference was supported by The WALTHAM Centre for Pet Nutrition and organized in collaboration with the University of California, Davis, and Cornell University. This publication was supported by The WALTHAM Centre for Pet Nutrition. Guest editors for this symposium were D'Ann Finley, Francis A. Kallfelz, James G. Morris, and Quinton R. Rogers. Guest editor disclosure: expenses for the editors to travel to the symposium and honoraria were paid by The WALTHAM Centre for Pet Nutrition.

² Author disclosure: Lodging expenses at the symposium for the corresponding author were paid by the WALTHAM Centre for Nutrition.

³ Supported by Kao Corporation and the Mark L. Morris Professorship in Clinical Nutrition, Texas A&M University.

⁵ Abbreviations used: ß-HB, ß-hydroxyburyrate; DAG, diacylglycerol; EDTA, ethylenediaminetetraacetate; GI, glycemic index; HGI, high glycemic index; HL, hepatic lipase; LGI, low glycemic index; LPL, lipoprotein lipase; MAG, monoacylglycerol; NEFA, nonesterifed fatty acid; TAG, triacylglycerol.

	LITERATURE CITED

TOP MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

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2. Murata M, Hara K, Ide T. Alteration by diacylglycerols of the transport and fatty acid composition of lymph chylomicrons in rats. Biosci Biotechnol Biochem. 1994;58:1416–9.

3. Murata M, Ide T, Hara K. Reciprocal responses to dietary diacylglycerol of hepatic enzymes of fatty acid synthesis and oxidation in the rat. Br J Nutr. 1997;77:107–21.[Medline]

4. Nagao T, Watanabe H, Goto N, Onizawa K, Taguchi H, Matsuo N, Yasukawa T, Tsushima R, Shimasaki H, Itakura H. Dietary diacylglycerol suppresses accumulation of body fat compared to triacylglycerol in men in a double-blind controlled trial. J Nutr. 2000;130:792–7.[Abstract/Free Full Text]

5. Maki KC, Davidson MH, Tsushima R, Matsuo N, Tokimitsu I, Umporowicz DM, Dicklin MR, Foster GS, Ingram KA, et al. Consumption of diacylglycerol oil as part of a reduced energy diet enhances loss of body weight and fat in compared to triacylglycerol control oil. Am J Clin Nutr. 2002;76:1230–6.[Abstract/Free Full Text]

6. Flicklinger BD. The effect of diacylglycerols on energy expenditure and substrate utilization in humans. In: Katsuragi Y, Yasukawa T, Matsuo N, Flickinger BD, Toimitsu I, Matlok MG, editors. Diacylglycerol oil. Champaign: American Oil Chemists' Society; 2004. p. 58–63.

7. Murase T, Aoki M, Wakisaka T, Hase T, Tokimitsu I. Anti-obesity effect of dietary diacylglycerol in C57L/6J Mice: Dietary diacylglycerol stimulates intestinal lipid metabolism. J Lipid Res. 2002;43:1312–9.[Abstract/Free Full Text]

8. Watanabe H, Tokimitsu I. Digestion and absorption of diacylglycerol. In: Katsuragi Y, Yasukawa T, Matsuo N, Flickinger BD, Toimitsu I, Matlok MG, editors. Diacylglycerol oil. Champaign: American Oil Chemists' Society; 2004. p. 30–45.

9. Butterwick RF, McConnell M, Markwell PJ, Watson TDG. Influence of age and sex on plasma lipoid and lipoprotein concentrations and associated enzyme activities in cats. Am J Vet Res. 2001;62:331–6.[Medline]

10. Umeda T, Bauer JE, Otsuji K. Weight loss effect of dietary diacylglycerol in obese dogs. J Anim Physiol Anim Nutr. 2006; in press.

11. Van Harmelen V, Reynisdottir S, Cianflone K, Degerman E, Hoffstedt J, Nilsel K, Sniderman A, Arner P. 1999. Mechanisms involved in the regulation of free fatty acid release from isolated human fat cells by acylation-stimulating protein and insulin. J Biol Chem. 274:18243–51.[Abstract/Free Full Text]

12. Goda T, Urakawa T, Watanabe M, Takase S. Effect of high-amylose starch on carbohydrate digestive capacity and lipgenesis in epididymal adipose tissue and liver of rats. 1994. J Nutr Biochem. 5:256–260.

13. Kishida T, Nogami H, Himeno S, Ebihare K. Heat moisture treatment of high amylose cornstarch increases it resistant starch content but not is physiologic effect in rats. J Nutr. 2001;131:2716–21.[Abstract/Free Full Text]

14. Nikkila EA, Huttunen JK, Ehnholm C. Postheparin plasma lipoprotein lipase and hepatic lipase in diabetes mellitus. Relationship to plasma triglyceride metabolism. Diabetes. 1977;26:11–21.[Abstract]

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