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* Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 23610; Department of Small Animal Medicine and Surgery, College of Veterinary Medicine Texas A&M University, College Station, TX 77843; ** Alpo Petfoods, Inc., Allentown, PA 18001, AZ 85262; and School of Statistics, University of Minnesota, Minneapolis, MN 55455
4 To whom correspondence should be addressed. Email: hillr{at}mail.vetmed.ufl.edu.
KEY WORDS: • protein • soy • glucose • insulin • dogs
Foods that stimulate a lower glycemic response are recommended for patients with diabetes. In humans, consumption of sugar results in larger increases in postprandial blood glucose concentrations than does consumption of less easily digested carbohydrates (1). In dogs, blood glucose increased markedly when soft, moist diets containing corn syrup were fed, but the mean increase or decrease was <1 mmol/L when dry and canned diets were fed (2,3). Postprandial glucose and insulin responses in dogs fed canned and dry diets correlated positively with dietary starch and negatively with dietary fat; the insulin response correlated positively with dietary protein (4). Both glucose and insulin responses were affected by the source of starch (5).
All these dog studies compared blood glucose and insulin concentrations for <4 h after a meal and insulin concentrations appeared not to have returned to baseline by the end of the study. A short 2-h period of blood sampling could be sufficient to assess the response to a meal that produces a rapid increase in blood glucose (6), but the hormonal response to a complex meal may last for 12–24 h in dogs (7,8). The duration of the hormonal response is shorter after smaller meals, but the duration is similar whether food is fed as a single meal or divided and fed as 2 meals (7). Thus, normal dogs closely regulate blood glucose concentrations by prolonging absorption and matching glucose appearance with glucose disappearance. Insulin secretion must respond to other stimuli such as blood amino acid concentrations (9,10). In dogs, measuring blood glucose may be of little benefit, therefore, when assessing the effect of food composition on the hormonal response to a meal, and insulin may need to be measured for >4 h after a meal.
Both soluble and insoluble fibers have been shown to reduce the postprandial glycemic response in diabetic dogs that are fed low fat diets (11,12) but the effect of fiber in high fat diets is unknown. Dietary fat is a more potent inhibitor of gastric emptying and intestinal motility than fiber. In humans, infusing fat into the duodenum stimulates cholecystokinin secretion, which slows gastric emptying and markedly reduces the glucose and insulin response to oral glucose (13). The effect of fiber on the hormonal response to high fat foods needs to be assessed.
Texturized vegetable protein from soy (TVP)6 is commonly included in commercial dog foods because it retains the appearance of meat during canning. This TVP is an economical source of protein but also contains carbohydrate (oligosaccharides and polysaccharides) only some of which (sucrose and starch) are digestible. The polysaccharides are mostly composed of a pectin-like acidic polysaccharide and an arabinogalactan, both of which could influence gastric emptying, digestion, or absorption (14). Previously, we have shown in dogs that the prececal digestibility of protein from TVP is only slightly less than that of beef protein but that the prececal digestibility of nitrogen-free extract (NFE), representing carbohydrate, is much reduced in high TVP diets (14). The purpose of this study, therefore, was to examine the effect of increasing amounts of TVP on postprandial blood glucose and insulin concentrations for 6–12 h after high-fat canned diets were fed to dogs.
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MATERIALS AND METHODS |
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77% moisture and, on a dry matter basis, 5.7 Mcal/kg gross energy, 23% crude protein, 32% crude fat, 31% NFE, and 1% crude fiber. Nevertheless, the proportion of dietary protein from TVP:beef was 0:100, 14:86, 29:71, and 57:43, respectively, and the amount of NFE from TVP increased and the amount of NFE from corn starch decreased as TVP increased in the diets. A previous study using the same batch of food and similar dogs had established that increasing amounts of NFE from these diets were not digested in the small intestine (20, 26, 29, and 38%, respectively) and total gut energy digestibility decreased slightly from 92 to 89% as TVP increased in the diet (14). Dogs were fed a single meal in an amount that maintained body weight, and the amount fed was the same by weight for each diet. The amount to feed was determined during a 2-wk acclimatization period during which dogs were fed the diet with a TVP:beef protein ratio of 14:86. On d 7 of each diet treatment period, a catheter was inserted into a cephalic vein and blood samples were obtained before and 30, 60, 90, 120, 180, 240, 300, and 360 min after the daily meal. In 6 dogs, samples were also obtained 7, 8, 10, and 12 h after the meal. Samples were collected in evacuated tubes containing sodium fluoride and potassium oxalate for analysis of glucose and containing no anticoagulant for analysis of insulin. Samples were centrifuged immediately; plasma and serum were stored at –20°C until analysis. Insulin concentrations were measured by radioimmunoassay using a commercial kit (Coat-A-Count Insulin, DPC) that has been previously validated in dogs (16). Glucose concentrations were measured spectrophotometrically using a hexokinase method (Glucose (HK), Sigma Diagnostics).
Results are reported as means ± SD. The area under curve (AUC) of insulin and glucose concentrations was determined by summing trapeziums beneath straight lines joining adjacent concentrations. Values were log transformed before analysis. Data were analyzed for 10 dogs up to 6 h after the meal as a 4-period crossover design with time as a within-period repeated-measures factor, using generalized least squares estimation (SAS system for windows, version 9.0) (17). An autoregressive covariance structure was used to explicitly model the correlation between measurements over time and a random effect for each dog was included. We included diet and period as factors and also tested for diet-by-period and diet-by-time interactions. Slices of data at each time point and for each diet were compared. The AUC of insulin and glucose over 2, 6, and 12 h, body weight, and the average amount of food consumed daily was compared among diets using a repeated measure ANOVA. Post hoc comparisons were performed with a Bonferroni correction. A probability of error of 0.05 was considered significant and the power of the study was 80% to detect a difference in concentration of 0.6 mmol/L of glucose, 10 µ IU/mL of insulin, or 45% change in AUC of insulin and a 10% change in AUC of glucose in 10 dogs. Data were also analyzed for 6 dogs over 12 h.
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RESULTS |
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DISCUSSION |
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TOPMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In dogs fed the highest TVP diet, insulin secretion was lower for 2–3 h after a meal but there was an irregular but substantial secretion of insulin after 3 h. As a result, TVP did not affect the AUC of insulin over 6 or 12 h but mean insulin concentrations over 6 h were 20% higher in dogs fed the all-beef protein diet. A more subtle change in AUC of insulin may have been detected if more dogs were studied because the variance of AUC of insulin was large and the power of the study was only sufficient to detect a 45% difference. Nevertheless, measurement over a longer period suggested a more modest response than measurement over a shorter period. This suggests that a longer period of study (>7 h) is needed to evaluate the insulin response to large meals of complex high fat foods in dogs, though shorter periods may be sufficient for smaller meals (7,8).
Soy carbohydrate is probably responsible for the effects observed in this experiment. Soy protein in these diets is only slightly less digestible than beef protein, whereas there were more substantial differences in the digestibility of carbohydrates (14). Forms of soy that contain soy carbohydrate may, therefore, have some utility in helping to regulate hyperglycemia in dogs with diabetes. Nevertheless, fecal consistency also changed as TVP was added to the diet from very firm when the 100% beef protein diet was fed to soft or liquid when the high TVP diet was fed (14). This was associated with an increase in fecal water content and increased quantities of feces. This change in fecal consistency could limit the amount of TVP that may be added to a diet.
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FOOTNOTES |
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2 Author disclosure: Expense for R.C. Hill to travel to the symposium and honoraria were paid by The WALTHAM Centre for Pet Nutrition. R.C. Hill is The WALTHAM Associate Professor of Small Animal Internal Medicine and Nutrition at the University of Florida. J.E. Bauer's lodging expenses at the symposium were paid for by The WALTHAM Centre for Pet Nutrition.
3 Funding was provided by Archer Daniels Midland, Alpo Petfoods, and the Alpo Research Fellowship.
5 Present address: 6811 E. Horned Owl Trail, Scottsdale, AZ 85262.
6 Abbreviations used: TVP, texturized vegetable protein; NFE, nitrogen free extract; AUC, area under curve.
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LITERATURE CITED |
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1. Mann J. Carbohydrates. In: Bowman BA, Russell RM, editors. Present knowledge in nutrition. 8th ed. Washington, DC: International Life Sciences Institute; 2001. p. 59–71.
2. Holste LC, Nelson RW, Feldman EC, Bottoms GD. Effect of dry, soft moist, and canned dog foods on postprandial blood glucose and insulin concentrations in healthy dogs. Am J Vet Res. 1989;50:984–9.[Medline]
3. Nguyen P, Dumon H, Buttin P, Martin L, Gouro AS. Composition of meal influences changes in postprandial incremental glucose and insulin in healthy dogs. J Nutr. 1994;124:2707S–11S.
4. Nguyen P, Dumon H, Biourge V, Pouteau E. Glycemic and insulinemic responses after ingestion of commercial foods in healthy dogs: influence of food composition. J Nutr. 1998;128:2654S–8S.
5. Sunvold GD, Bouchard GF. The glycemic response to dietary starch. In: Reinhart GA, Carey DP, editors. Recent advances in canine and feline nutrition, Vol 2, Iams nutrition symposium proceedings.Wilmington, OH: Orange Frazer Press; 1998. p. 123–31.
6. Nguyen P, Dumon H, Biourge V, Pouteau E. Measurement of postprandial incremental glucose and insulin changes in healthy dogs: influence of food adaptation and length of time of blood sampling. J Nutr. 1998;128:2659S–62S.
7. Nomura M, Greenberg GR, Bahoric A, Zinman B, Albisser AM. How laboratory dogs accommodate meals of different size but similar composition. Am J Physiol. 1985;248:E101–7.
8. Goriya Y, Bahoric A, Marliss EB, Zinman B, Albisser AM. Diurnal metabolic and hormonal responses to mixed meals in healthy dogs. Am J Physiol. 1981;240:E54–9.
9. Strack TR, Poussier P, Marliss EB, Albisser AM. Glucose turnover after a mixed meal in dogs: glucoregulation without change in arterial glycemia. Am J Physiol. 1994;266:R889–95.
10. Albisser AM, Cheng DC, Yamasaki Y, Marliss EB, Zinman B. Changes in blood amino acids account for the insulin and glucagon responses to mixed meals in dogs. Diabetes Res. 1985;2:49–55.[Medline]
11. Nelson RW, Ihle SL, Lewis LD, Salisbury SK, Miller T, Bergdall V, Bottoms GD. Effects of dietary fiber supplementation on glycemic control in dogs with alloxan-induced diabetes mellitus. Am J Vet Res. 1991;52:2060–6.[Medline]
12. Kimmel SE, Michel KE, Hess RS, Ward CR. Effects of insoluble and soluble dietary fiber on glycemic control in dogs with naturally occurring insulin-dependent diabetes mellitus. J Am Vet Med Assoc. 2000;216:1076–81.[Medline]
13. Liddle RA, Rushakoff RJ, Morita ET, Beccaria L, Carter JD, Goldfine ID. Physiological role of cholecystokinin in reducing postprandial hyperglycemia in humans. J Clin Invest. 1988;81:1675–81.[Medline]
14. Hill RC, Burrows CF, Ellison GW, Bauer JE. The effect of texturized vegetable protein from soy on nutrient digestibility compared to beef in cannulated dogs. J Anim Sci. 2001;79:2162–71.
15. National Research Council. Guide for the care and use of laboratory animals. Publication no. 85–23 (rev.). National Institutes of Health, Washington, DC; 1985.
16. Wolfsheimer KJ, Flory W, Williams MD. Effects of prednisolone on glucose tolerance and insulin secretion in the dog. Am J Vet Res. 1986;47:1011–4.[Medline]
17. Littell RC, Milliken GA, Stroup WW, Wolfinger RD. SAS system for mixed models. Cary, NC: SAS Institute Inc.; 1996.
18. Hill RC, Burrows CF, Ellison GW, Bauer JE. The effect of texturized vegetable protein containing soy carbohydrate on oroileal transit of chromic oxide in cannulated dogs. J Anim Sci. 2000;78:2633–8.
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