The Journal of Nutrition Vol. 128 No. 12 December 1998, pp. 2654S-2658S

Glycemic and Insulinemic Responses after Ingestion of Commercial Foods in Healthy Dogs: Influence of Food Composition^1,2

Patrick Nguyen³, Henri Dumon, Vincent Biourge^*, and Etienne Pouteau

Department of Nutrition, École Nationale Vétérinaire de Nantes, 44307 Nantes Cedex 03, France and ^* Royal Canin Research Centre, 56007 Vannes Cedex, France

KEY WORDS: dog foods · analytical composition · food processing · glycemic response · insulinemic response · dogs

	INTRODUCTION

Introduction References

Great variations in the postprandial glucose concentration and insulin secretory responses to different foods have been shown in dogs (Holste and al. 1989, Nguyen and al. 1994). It has been suggested that foods yielding low glycemic responses would be recommended for diabetic or obese subjects and in the prevention of many other disorders. High carbohydrate/high fiber diets enhance peripheral glucose disposal and decrease insulin requirements in insulin-dependent diabetic subjects. In overweight patients with noninsulin-dependent diabetes mellitus (NIDDM),⁴ reducing diet glycemic response improves overall blood glucose control, long-term glycemic control and lipid control. Diets with a high glycemic response that are low in fiber increase the risk of NIDDM in humans. Foods with a low glycemic response combined with a high dietary fiber content decrease free fatty acid level, which is associated with abdominal obesity and cardiovascular risk. They cause rapid intestinal absorption of glucose into the blood, leading to postprandial hyperinsulinemia, which may play a role in promoting colon carcinogenesis. A diet high in refined carbohydrates and low in water-soluble fiber causes rapid absorption of glucose with similar results.

Because of the clinical implications of the glycemic index, notably in diabetes management or in dietary strategy to avoid or treat overweight or moderate obesity, the factors that affect it have been the subject of many studies (Wolever and al. 1991).

The extent of postprandial hyperglycemia and insulin secretion depends on the amount of food and carbohydrate consumed per meal. However, different kinds of carbohydrate elicit different glucose and insulin concentrations, because their chemical nature, especially the ratio of amylose to amylopectin forms of starch, may affect their rate and speed of digestion. Dietary fiber slows down the rate of passage and the rate of hydrolysis of starchy polysaccharides (Wolever 1990). Dietary fat delays stomach emptying (Gulliford and al. 1989), and high intakes of rapidly digested proteins modify the glycemic response by increasing insulin secretion (Nuttall and Gannon 1990). The food processing may be of particular importance for dog food. The type of food, dry, canned or soft moist, affects the maximal postprandial glucose concentration as much as the time at which this peak occurs (Holste and al. 1989).

The glycemic index methodology is based on tests of single foods and could be applied to the testing of mixed meals. Nevertheless, its practical utility is controversial because differences among foods could be partially abolished in mixed meals by the effects of protein and fat. Whatever it may be, an individual food evaluation is not realistic in dogs. Their complete foods contain many components. There are large variations in their protein and fat content and the technological processes can largely modify the intrinsic carbohydrate availability.

Nevertheless, information concerning postprandial responses would be of great interest in regard to obesity. Along with a long-term excessive energy intake, food quality may play a significant role according to its humoral and metabolic effects. This information may also be of interest in the management of NIDDM (which elicits alteration of carbohydrate tolerance and insulin action) as much as insulin-dependent diabetes mellitus (IDDM; reduction of fluctuations in blood glucose, synchronization of glucose increase and insulin administration).

The purpose of this study was to determine how the differences in carbohydrate (starch and dietary fiber, soluble and insoluble), protein and fat content of complete (and complex) foods given to healthy dogs in a single meal on a normoenergetic basis modify their postprandial plasma glucose and insulin responses.

Material and methods.  Animals. Twelve adult (older than 15 mo) beagle dogs were studied, according to the French Ministry of Agriculture and Fisheries regulatory rules for animal welfare. They were allotted to two groups; from each group, five dogs were used alternately for tests, excluding in particular dogs that did not eat the entire meal that they were offered. None of the dogs was obese (13.5 kg mean body weight) and they were clinically normal. Their basal plasma glucose (5.21 ± 0.50 mmol/L) and their response to the intravenous glucose tolerance test (performed after a 24-h period of food deprivation, using a glucose dose of 500 mg/kg body weight, infused as 50% glucose solution in 30 s) were also normal.

These dogs were accustomed to the experimental procedure. They were commonly used for digestibility trials in the cages used in this study and had been previously subjected to repeated venipuncture. Therefore, their responses were due to the experimental variables and not to stress.

Experimental diets. Twenty experimental foods (C1-C5 and D1-D15) were tested. Foods D1- D15 were dry foods, whereas C1-C5 were canned. These test foods were intended to be representative of foods currently used for maintenance or for clinical purposes in adult dogs. They were designed to vary in macronutrient composition [15.4-62.6% crude protein (CP), 7.9-31.0% ether extract (EE), 3.2-39.1% total dietary fiber (TDF) and 0.4-52.7% starch (ST), on a dry matter basis]; the energy content was 965-2045 kJ/100 g dry matter. The composition of test meals is shown in Table 1. The daily chromium intake was not <100 µg per dog. (The requirement for chromium to maintain normal glucose tolerance has not been shown in dogs. However, a daily allowance of 100 µg per dog per day was assumed to be needed according to a human recommendation of 50-200 µg/d.)

Design and procedures. Before the initiation of the study, the dogs consumed in a single daily meal a standard dry food consisting of 29.3% CP, 11.2% EE, 11.0% TDF and 27.8% ST on a dry matter basis for at least 2 wk. After a 24-h period of food deprivation, they were again given, on the morning of the test days, in a single meal, one of the 20 experimental foods. The size of the meal was determined by the energy requirement of the individual dog [552 kJ metabolizable energy per kg metabolic body weight (BW^0.75)]. One hour before feeding time, each dog was placed in a separate cage, and a basal blood sample (after 24 h of food deprivation) was obtained from the jugular vein. Each dog consumed all of the food in <5 min. Further jugular vein blood samples were collected at the end of the meal (time 0) and 5, 10, 15, 20, 30, 45, 60 and 90 min later. Blood samples were taken in 5-mL heparinized vacuum collecting tubes and immediately refrigerated on ice. They were centrifuged at 600 × g for 15 min to separate the plasma, which was stored at 20°C until analysis. Plasma glucose concentrations were determined by an enzymatic kit (Glucose GOD-PAP, Boehringer-Mannheim, Germany). Plasma insulin was measured by RIA using a commercially available kit (human insulin as standard; Insik-5, Sorin Biomedica, Saluggia, Italy). Digestibility coefficients had been evaluated for CP, EE, organic matter and energy, for six foods in the same groups of dogs.

Calculations and statistics. Changes in serum glucose and insulin concentration were calculated separately for each postmeal period by using the serum concentration before the meal as a baseline. Postprandial responses were compared for maximum increase, time to peak increase and incremental area under the glucose (AUCG) and insulin (AUCI) curves for each food. The integrated AUCG and AUCI was calculated by the trapezoidal method for the 90-min period after the meal. The Multifit 2.01 software (Day Computing, Cambridge, UK) was used for computing the area under the curve. Multiple regressions with the experimentally determined AUCG and AUCI as the dependent variables and the different nutrient levels (CP, EE, TDF and ST) as independent variables were performed. The statistical program utilized was the multivariate general linear hypothesis procedure of Systat for Macintosh (Version 5.0, Evanston, IL).

Results.  Similar basal blood glucose and insulin were found before ingestion of the test meals. Average (means ± SEM) blood glucose and insulin area (above basal) over a 90-min period related to the 20 foods are shown in Table 2, as are the maximum postprandial glucose and insulin increments and the time after meal feeding at which these increments occurred. There was a wide range of variation in maximal glucose (0.0-1.8 mmol/L) and insulin (11-54 µU/L) increments above the basal value and in glycemic [mean AUCG 1.0-92.5 mmol/(L · min)] and insulin [mean AUCI 365-2874 µU/(L · min)] response.

A linear correlation between the ST content of the foods and the glucose response area was observed. The maximum blood glucose increment (MBGI) was positively correlated with AUCG and with ST content of the foods. It was negatively correlated with their EE content.

A linear correlation between the ST, CP and EE content of the diets and area under the postprandial insulin response curve was observed. The maximum blood insulin increment (MBII) was positively correlated with AUCI and with ST and CP content of the foods. It was also negatively correlated with their EE content. There was no correlation between either AUCG and AUCI or MBGI and MBII. Taking differences in CP, EE and dietary fiber (total, soluble and insoluble) content or digestibility coefficients or digestible energy and nutrient contents into account did not improve these results.

Discussion.  The foods tested in this study were chosen to represent the nutritional variability that can be observed in commercially available dog foods. The size of the test meal was selected to meet the daily energy requirement of the dog, without any consideration of the carbohydrate content. In addition, because the purpose of this study was to compare the effects of foods markedly different in their composition, no attempt was made to equalize protein, fat or fiber intakes. Because the diet consumed before the start of the study was the same in all cases, the differences in responses to test meals might have been minimized.

In humans, several studies have shown an effect of factors such as fat, protein, dietary fiber (Wolever et al. 1991), phytate and other antinutrients in influencing the glycemic and the endocrine responses. Our results suggest, at least in normal dogs over the range of foods tested, that the ST content of the diets is the primary determinant of postprandial glucose, whereas variations in diet CP and EE appear to have a negligible effect. In contrast, CP and EE as well as the ST content appear to determine the insulin response. In neither case was there any influence of the dietary fiber content of the foods.

A significant negative relationship has been shown between fat and protein and postprandial glucose rise but not with fiber or sugar content (Jenkins and al. 1981). The coingestion of large amounts of protein and fat results in a reduction of the difference between the glycemic response of foods (Gulliford and al. 1989). This effect of protein addition would be caused by an increase in the osmolality of the stomach contents, reducing the rate of gastric emptying. It also could be the consequence of the increase in the plasma insulin response.

Nevertheless, this relationship between protein ingestion and the glycemic response to carbohydrates appears to occur mainly in the case of protein addition to low protein starchy foods or to pure carbohydrate loads. The effects of adding protein and/or fat to a meal have been shown to be higher with foods in which carbohydrates were rapidly absorbed. (Gulliford and al. 1989). The removal of protein from wheat products results in a greater rise in blood glucose. Addition of gluten to gluten-free bread mix does not reverse these effects, suggesting the existence of natural starch-protein interactions (Jenkins and al. 1987). That may explain in part why we do not find any relationship between the protein content of the complete mixed dog foods and their glycemic responses. Canned foods have the highest protein content but on a dry matter basis contain little starch. Dry foods are generally balanced by mixing high protein/low starch and low protein/high starch ingredients. In neither case would there be any significant protein-starch interaction to counteract the effect of starch load.

Oral and enteral fat administration may delay upper gastrointestinal transit, as shown in humans (Gulliford and al. 1989), by reducing the rate of gastric emptying, the jejunal motility and the postprandial flow rates in the small intestine, hence flattening the glucose response. However, the effect of fat is more marked if the glycemic response is limited by the rate of gastrointestinal transit or by other factors such as the rate of starch hydrolysis. The addition of fat reduced the glycemic response to mashed potato but had no effect on the blood glucose response to spaghetti (Gulliford and al. 1989). Furthermore, the amount of fat required to have this effect was very large, i.e., 50 g fat to reduce markedly the glucose response to a 50-g carbohydrate load (Wolever and Bolognesi 1996). In other respects, the feeding of a high fat canned diet had no effect on gastric emptying time in dogs (Burrows and al. 1985), and Wolever and al. (1994) found that adding fat delayed the increase in plasma glucose but had no effect on the overall AUCG.

Both high insoluble-fiber (cellulose) and high soluble-fiber (pectin) diets lower the mean postprandial plasma glucose concentration measured for 24 h in diabetic dogs (Nelson and al. 1991). In humans, some results have shown a major effect of the insoluble fiber fraction (Wolever 1990). However, a strong dependency of glycemic index on soluble dietary fiber also suggests a major function of such fiber in the TDF hypoglycemic response. Soluble fiber, forming viscous solutions, flattens the postprandial glucose curve probably as a result of a slower gastric emptying and of a reduced rate of starch degradation by pancreatic -amylase, but these effects were reported mainly when purified forms of fiber were added to the meals (Leclere and al. 1994).

In most human studies conducted to examine the effects of the coingestion of protein, fat and dietary fiber with different sources of carbohydrate, the amount and source of carbohydrate remained the major determinants of the glycemic responses to a standardized or at least a similar amount of carbohydrate with and without co-ingestion. In this study, we compared the effects of differences in food composition, including differences in starch content but not its sources.

In humans, both the source and the amount of carbohydrate influence the postprandial glucose and insulin responses. The relationship between these responses and the ingested amount of carbohydrate has been shown to be nonlinear. A fourfold increment of carbohydrate ingestion led to only a 1.5- to twofold increase of the incremental AUCG and about a threefold increase of AUCI (Wolever and Bolognesi 1996) in normal subjects.

The physical structure of carbohydrate-containing foods can influence the rate of starch hydrolysis and, in turn, the postprandial glucose response. Any process that disrupts the physical or botanical structure of food ingredients, increases the plasma glucose and insulin responses, and modifies the extent of processing and the final degree of gelatinization may be a factor that determines the rate of starch digestion and the subsequent glycemic response. Extrusion is a very effective process that allows starch granules to be completely gelatinized during a short cooking time under high temperature/high pressure conditions. The structure of starch granules is destroyed, thus inducing higher susceptibility to -amylase degradation. A similar effect on the starch availability may be achieved in canned foods through appertization (sterilization under high moisture/high temperature conditions), which allows a high degree of starch cooking.

All of the dry foods tested contained exclusively extruded and expanded grains and oil-cake meals as starch sources; the canned diets were appertized. These processes may have abolished the initial differences in the susceptibility to -amylase and hence in the rate of in vivo starch hydrolysis. The absence of difference may have been strengthened by the higher gastrointestinal transit rate in dogs than in humans. Overall, this may explain why only the amount of ingested starch is shown to influence the glycemic response in dogs.

Furthermore, in our study, the dogs where fed according to their energy needs, hence there was no adjustment of the amount of ingested starch. Therefore, on a metabolic weight (BW^0.75) basis, they ingested about five times (10 g/kg BW^0.75) the amount of starch that was used as a comparison of the glycemic index methodology in humans (50 g per subject of about 70 kg BW, i.e., 2 g/kg BW^0.75). Together with the high glycemic index of extruded starch, this may constitute one of the reasons why we did not observe any protein, fat and dietary fiber influences on the glycemic response in adult dogs fed these types of foods on an energy requirement basis.

We conclude that the amount of starch consumed is the major determinant of the glucose response of adult healthy dogs to different complete diets that varied in their analytical composition and energy profile. Variations in CP, EE and DF, over the range tested here, appear to have a negligible effect on postprandial glucose response. The maximal blood glucose increment is also determined by the ST content but is also negatively correlated to the EE content. This may be due to the delaying of gastric emptying. Both the insulin response and the maximal blood insulin increment depend on the ST, CP and EE content of foods. As shown in human studies, the ST effects could be modulated by the effects of protein (amino acids) on insulin secretion and EE on upper gastrointestinal transit rate. These results could be of interest in the management of some common nutritional disorders in dogs such as obesity and NIDDM.

	FOOTNOTES

	LITERATURE CITED

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