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Substrate source utilization during moderate intensity exercise with glucose ingestion in Type 1 diabetic patients

¹Département de chimie-biologie et des sciences de l'activité physique, Université du Québec à Trois-Rivières, Trois-Rivières; ²Division de kinésiologie et Unité de recherche en diabète, Université Laval, Québec City; ³Département de kinésiologie, Université de Montréal, Montréal; and ⁴Département de kinanthropologie, Université du Québec à Montréal, Montréal, Québec, Canada

Submitted 31 December 2006 ; accepted in final form 10 April 2007

	ABSTRACT

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Substrate oxidation and the respective contributions of exogenous glucose, glucose released from the liver, and muscle glycogen oxidation were measured by indirect respiratory calorimetry combined with tracer technique in eight control subjects and eight diabetic patients (5 men and 3 women in both groups) of similar age, height, body mass, and maximal oxygen uptake, over a 60-min exercise period on cycle ergometer at 50.8% (SD 4.0) maximal oxygen uptake [131.0 W (SD 38.2)]. The subjects and patients ingested a breakfast (containing 80 g of carbohydrates) 3 h before and 30 g of glucose (labeled with ¹³C) 15 min before the beginning of exercise. The diabetic patients also received their usual insulin dose [Humalog = 9.1 U (SD 0.9); Humulin N = 13.9 U (SD 4.4)] immediately before the breakfast. Over the last 30 min of exercise, the oxidation of carbohydrate [1.32 g/min (SD 0.48) and 1.42 g/min (SD 0.63)] and fat [0.33 g/min (SD 0.10) and 0.30 g/min (SD 0.10)] and their contribution to the energy yield were not significantly different in the control subjects and diabetic patients. Exogenous glucose oxidation was also not significantly different in the control subjects and diabetic patients [6.3 g/30 min (SD 1.3) and 5.2 g/30 min (SD 1.6), respectively]. In contrast, the oxidation of plasma glucose and oxidation of glucose released from the liver were significantly lower in the diabetic patients than in control subjects [14.5 g/30 min (SD 4.3) and 9.3 g/30 min (SD 2.8) vs. 27.9 g/30 min (SD 13.3) and 21.6 g/30 min (SD 12.8), respectively], whereas that of muscle glycogen was significantly higher [28.1 g/30 min (SD 15.5) vs. 11.6 g/30 min (SD 8.1)]. These data indicate that, compared with control subjects, in diabetic patients fed glucose before exercise, substrate oxidation and exogenous glucose oxidation overall are similar but plasma glucose oxidation is lower; this is associated with a compensatory higher utilization of muscle glycogen.

indirect respiratory calorimetry; carbon isotopes; insulin; muscle glycogen; plasma glucose oxidation

In the present study, substrate oxidation during a 60-min exercise period at 50% O_max after ingestion of 30 g of glucose was compared in diabetic patients receiving their usual insulin dose and in control subjects. The glucose ingested was artificially labeled with ¹³C to compute the oxidation of exogenous glucose, plasma glucose, glucose released from the liver, and muscle glycogen from calorimetry data and ¹³CO₂ production at the mouth, and from the ¹³C enrichment of plasma glucose (3, 5, 6, 9, 20). On the basis of data from Krzentowski et al. (11) and Riddell et al. (24), we hypothesized that, during exercise, exogenous and endogenous CHO oxidation, respectively, will not be different in the diabetic patients and control subjects. However, Raguso et al. (21) have shown that, compared with control subjects, in response to a 30-min exercise period at 45% O_max without glucose ingestion, the rate of plasma glucose disappearance was lower in diabetic patients, presumably because of a defective recruitment of glucose transporters. In addition, recent data from Chokkalingam et al. (4) suggest that the oxidation rate of plasma glucose in diabetic patients during exercise could be lower than its rate of disappearance. From these results and from the observation that endogenous CHO oxidation during exercise with glucose ingestion was not significantly different in diabetic patients and control subjects (11, 24), we hypothesized that the oxidation of plasma glucose and of glucose released from the liver could be lower, whereas that of muscle glycogen could be higher in diabetic patients than in control subjects.

	METHODS

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Eight control subjects and eight diabetic patients (5 men and 3 women in each group), with similar average age, height, body mass, and O_max on cycle ergometer (Table 1), gave their written informed consent to participate in this study. The study was approved by the Ethic Committees on the use of human subjects in research of the Université Laval and the Université du Québec à Trois-Rivières. Both control subjects and diabetic patients were lean, nonsmokers and were moderately active (2–5 h/wk). The women in both groups were taking oral contraceptives and were studied in the follicular phase of the menstrual cycle (5–7 days after the beginning of menstruation). Insulinotherapy for the diabetic patients included the insulin analog Humalog (Lispro, Eli Lilly Canada, Scarborough, Ontario, Canada) before every meal and Humulin N (Eli Lilly Canada) before breakfast and at bedtime. The concentration of glycated hemoglobin (Table 1) indicated that, at the time of experiment, the patients were in good metabolic control and all of them were free of diabetic complications as assessed by their physicians. No episode of hypoglycemia was reported by the diabetic patients for at least 24 h before the experiment. During the 2 days preceding the experiment, all subjects refrained from exercising and from ingesting alcohol and caffeine. They also avoided ingesting foods containing CHO with a high ¹³C content (e.g., corn, sugar cane), which may modify the background ¹³C enrichment of plasma glucose and expired CO₂ (12). On the day before the experiment, the evening meal was standardized and taken between 0700 and 0800 (13 kcal/kg; 20% proteins, 35% lipids, and 45% CHO).

A 30-g glucose load dissolved in 300 ml of water was ingested 15 min before the beginning of exercise. The glucose derived from corn (Biopharm, Laval, Canada; ¹³C/¹²C = –11.0 [-¹³C]PDB) was artificially enriched with [U-¹³C]glucose (¹³C/C > 99%; Isotec, Miamisburg, OH) to achieve a final isotopic composition of 400 [-¹³C]PDB. This high ¹³C enrichment of exogenous glucose provides a strong signal in plasma glucose as well as in expired CO₂ and allows the neglect of the comparatively small changes in background enrichment of expired CO₂ observed from rest to exercise (19).

Observations were made at rest before glucose ingestion, before the beginning of exercise, and every 15 min during the exercise period. Fat and CHO oxidation were computed from indirect respiratory calorimetry corrected for protein oxidation. For this purpose, oxygen consumption (O₂) and carbon dioxide production (CO₂) were measured by open-circuit spirometry (5-min collection period), and urea excretion in urine was measured over 5 h (from 7:30 AM to 12:30 PM). For the measurement of the isotopic composition (¹³C/¹²C) of expired CO₂, 10-ml samples of expired gas were collected in vacutainers. Finally, at rest before ingestion of [¹³C]glucose and at regular intervals during the exercise period, 10-ml blood samples were withdrawn through a catheter (Cathlon Clear, Johnson & Johnson), which was placed in an antecubital vein at the beginning of the experiment, for the measurement of plasma glucose and insulin concentrations and of ¹³C/¹²C in plasma glucose. Between the samplings that were made, the catheter was kept patent by a slow infusion of sterile isotonic saline.

Plasma samples were stored at –80°C until analyses. In addition, in diabetic patients, plasma glucose concentration was measured at 5-min intervals throughout the period of exercise and the 60-min recovery period to verify that hypoglycemia did not develop (One Touch Ultra glucose meter; LifeScan, Milpitas, CA).

Substrate oxidation was computed from O₂ and CO₂ (in l/min) (18):

(1)

(2)

In these computations, O₂ and CO₂ were corrected for the average rate of protein oxidized over the 5-h period of observation [38 mg/min (SD 12) and 35 mg/min (SD 10) in control subjects and diabetic patients; not significantly different].

Plasma glucose ¹³C/¹²C was measured as previously described (3). Briefly, plasma glucose was separated by double-bed ion-exchange chromatography (AG 50W-X8 H⁺ and AG 1-X8 chloride, 200–400 mesh; Bio-Rad, Mississauga, ON, Canada) after deproteinization with barium hydroxide and zinc sulfate (0.3 N). The eluate was evaporated to dryness (Virtis Research Equipment, New York, NY) and combusted (60 min at 400°C with copper oxide), and the CO₂ was recovered for the isotopic analyses.

Measurement of ¹³C/¹²C in expired CO₂ and in CO₂ from combustion of plasma glucose was performed by mass spectrometry (Prism, Manchester, UK). The isotopic composition of ingested glucose, expired CO₂, and plasma glucose was expressed in difference by comparison with the PDB Chicago Standard: [-¹³C]PDB-1 = [(Rspl/Rstd) – 1] x 1,000, where Rspl and Rstd are the ¹³C-to-¹²C ratios in the sample and standard (1.1237%), respectively (3).

The oxidation rate of exogenous glucose (in g/min) was computed as follows (19):

(3)

In this equation, CO₂ (not corrected for protein oxidation) is in liters per minute, Rexp is the observed isotopic composition of expired CO₂, Rref is the isotopic composition of expired CO₂ at rest before ingestion of [¹³C]glucose, Rexo is the isotopic of the exogenous glucose ingested, and k (0.747 l/g) is the volume of CO₂ provided by the complete oxidation of glucose. In addition, based on the isotopic composition of plasma glucose (Rglu), the oxidation rate of plasma glucose (in g/min) was computed as follows (5, 20):

(4)

The oxidation rate of muscle glycogen (in g/min), either directly or through the lactate shuttle (2), was computed by the difference between the rate of total glucose oxidation (Eq. 1) and the oxidation rate of plasma glucose (Eq. 4). Finally, the oxidation rate of glucose released by the liver was estimated by the difference between the oxidation rate of plasma and exogenous glucose. These computations are based on the observation that, during exercise, ¹³C provided from [¹³C]glucose is not irreversibly lost in pools of tricarboxylic acid cycle intermediates and/or bicarbonate and that ¹³CO₂ recovery in expired gases is thus complete or almost complete (25, 29). However, the ¹³C/¹²C in expired CO₂ only slowly equilibrates with ¹³C/¹²C in the CO₂ produced in tissues (17). To take into account the delay between ¹³CO₂ production in tissues and at the mouth, exogenous and plasma glucose oxidation and oxidation of glucose released from the liver and muscle glycogen were only computed during the last 30 min of exercise, thus allowing for a 30-min equilibration period.

Plasma glucose concentration was measured by a spectrophotometric assay (Sigma Diagnostics, Mississauga, ON, Canada), whereas plasma insulin concentration was measured with a radioimmunoassay (KTSP-11001, Immunocorp Sciences, Montreal, QC, Canada).

Results are presented as means (SD). Comparisons were made by one-way or two-way ANOVA (diabetic patients vs. control subjects x time) with repeated measures on one factor (time). When appropriate, Newman-Keuls post hoc tests were performed. The comparisons were made at the 0.05 level of significance.

	RESULTS

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No significant difference was observed for gas exchanges between control subjects and diabetic patients at rest and during the exercise period (Table 2). In both groups, the contribution of CHO oxidation to the energy yield significantly decreased, whereas that of fat oxidation significantly increased from minutes 0–30 to minutes 30–60 during the exercise period (Table 3). However, the oxidation of CHO and fat and their respective contributions to the energy yield were not significantly different in control subjects and in diabetic patients.

View larger version (24K): [in this window] [in a new window]   Fig. 1. Isotopic composition (13C/12C) of expired CO2 (Rexp; bottom) and plasma glucose (Rglu; top) and percentage of plasma glucose arising from exogenous glucose (top) after [13C]glucose ingestion in control subjects and diabetic patients. Values are means and SD; n = 8 subjects. *Significantly different in the control subjects and diabetic patients (main effect with interaction for Rglu and Rexp) and significantly different from the control subjects by two-way ANOVA (group x time) with repeated measures on one factor (time): P < 0.05.

View larger version (31K): [in this window] [in a new window]   Fig. 2. Oxidation of glucose from various sources between minute 30 and 60 during exercise in control subjects and diabetic patients. Values are means and SD; n = 8 subjects. Exog, exogenous. *Significantly different from the control subjects by one-way ANOVA for independent measures: P < 0.05.

Table 4 and Fig. 2 show that, over the last 30 min of exercise, compared with the observations in control subjects, the oxidation of plasma glucose and of glucose released from the liver and their respective contribution to the energy yield were 50–55% lower in diabetic patients. In contrast, the oxidation of muscle glycogen and its contribution to the energy yield were significantly 250% higher.

In control subjects, plasma glucose concentrations significantly increased in response to glucose ingestion [from 4.8 mmol/l (SD 0.7) to 6.1 mmol/l (SD 1.3) at minute 15 during the exercise period] and then returned to preingestion levels (Fig. 3). In diabetic patients, plasma glucose concentration, which was significantly higher than in control subjects over the entire period of observation (main effect), also significantly increased in response to glucose ingestion [from 9.6 mmol/l (SD 2.9) to 11.7 mmol/l (SD 3.1) at minute 15 during the exercise period] but then significantly decreased below the value observed at rest before exercise [7.5 mmol/l (SD 3.4) at the end of exercise period]. In control subjects, glucose ingestion transiently increased plasma insulin concentration over basal values at minute 0. In diabetic patients, plasma insulin concentration was significantly higher than that shown in control subjects at rest and exercise (main effect) and slowly decreased over the observation period (Fig. 3).

View larger version (21K): [in this window] [in a new window]   Fig. 3. Plasma glucose (bottom) and insulin (top) concentrations in control subjects and diabetic patients. Values are means and SD; n = 8 subjects. *Significantly different from the corresponding peak value and significantly different in control subjects and diabetic patients (main effect with interaction for both variables) by two-way ANOVA (group x time) with repeated measures on one factor (time): P < 0.05.

	DISCUSSION

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In the studies by Krzentowski et al. (11) and by Riddell et al. (24), the glucose ingested was labeled with ¹³C to measure exogenous glucose oxidation. In both studies, the progressive increase in production of ¹³CO₂ at the mouth was slower and reached its maximum later in diabetic patients (11, 24); in the study by Riddell et al. (24), the percent contribution of exogenous glucose oxidation to the energy yield was significantly lower in diabetic patients than in control subjects. However, the amount of exogenous glucose oxidized over the exercise period was only slightly and not significantly lower in diabetic patients than in control subjects (11, 24). Because total CHO oxidation was not significantly different in diabetic patients and control subjects, endogenous glucose oxidation was not significantly different in the two groups described in Krzentowski et al. (11) and Riddell et al. (24). Results from the present experiment confirm these findings. The appearance of ¹³C in expired CO₂ was delayed over the first 30 min of exercise; however, over the second part of exercise (minutes 30–60), the amount of exogenous glucose oxidized, and its contribution to the energy yield was not significantly different in the diabetic patients and control subjects. Endogenous glucose oxidation was also similar over the last 30-min period of exercise in diabetic patients and in control subjects [37 g/30 min (SD 18) vs. 33 g/30 min (SD 14), contributing 54% (SD 13) vs. 49% (SD 11) to the energy yield, respectively]. These results from Krzentowski et al. (11) and Riddell et al. (24) and from the present experiment together show that, in diabetic patients receiving insulin, overall fuel selection, including the oxidation of exogenous glucose, is not different from that observed in control counterparts.

We are not aware of any study of plasma glucose oxidation during prolonged moderate exercise in Type 1 diabetic patients, and there are only a limited number of studies of the rate of plasma glucose disappearance (4, 21, 26, 27, 32). In addition, all of these studies have been conducted without administration of glucose, except for the recent study by Chokkalingam et al. (4), which was conducted under a slightly hyperglycemic (8 mmol/l)-hyperinsulinemic clamp. No significant differences were observed for rates of plasma glucose disappearance between control subjects and diabetic patients in work by Shilo et al. (26), Zinman et al. (32), and Simonson et al. (27). In contrast, in the study by Raguso et al. (21), the increase in rate of plasma glucose disappearance was similar in diabetic patients and in control subjects at 75% O_max but was 50% lower in diabetic patients than in control subjects at 45% O_max. In addition, data from Chokkaligam et al. (4) suggest that, in diabetic patients, plasma glucose oxidation could be much lower than its rate of disappearance. Unfortunately, no control subjects were included in that study. In line with these observations, in the present experiment, despite higher plasma glucose and insulin concentrations in diabetic patients than in control subjects, the oxidation of plasma glucose and that of glucose derived from the liver (Table 4), as well as their respective contributions to the energy yield (Fig. 2), were much lower in the diabetic patients than in control subjects. As discussed by Raguso et al. (21) and Chokkalingam et al. (4), this is probably due to a defect in insulin-mediated glucose transport in the muscle fiber in patients with Type 1 diabetes. This hypothesis is supported by data from Klip et al. (10) in rats with streptozotocin-induced diabetes. Compared with control rats, the number of GLUT4 transporters in the intracellular pool was lower and their redistribution on plasma membrane after insulin stimulation was also lower. As a consequence, insulin-stimulated glucose uptake was also 50% lower. Nuutila et al. (16) and Yki-Jarvinen et al. (31) also showed that insulin-stimulated muscle plasma glucose uptake was 25–45% lower in Type 1 diabetic patients than in control subjects.

In the present experiment, total CHO oxidation was not significantly different in the two groups, indicating a larger oxidation of glucose derived from muscle glycogen, which compensated for the lower oxidation rate of plasma glucose in the diabetic patients (Table 4 and Fig. 2). This observation differs from that of Raguso et al. (21), in which the reduction in plasma glucose oxidation (assumed to be equal to rate of plasma glucose disappearance) was compensated for by an increased intramuscular triglyceride oxidation, whereas muscle glycogen oxidation was not significantly different in diabetic patients and control subjects. Standl et al. (28) also reported that the reduction in muscle glycogen content over a 60-min exercise period at 50–60% O_max without glucose ingestion was not significantly different in well-controlled diabetic patients and in control subjects. However, the diabetic patients but not the control subjects ingested 36 g of CHO during the exercise period, and this could have resulted in muscle glycogen sparing. As for the difference between results from the present experiment and from that by Raguso et al. (21), it could stem from the fact that, in Raguso et al., the two groups were studied after a 12-h fast, whereas in the present experiment the diabetic patients and the control subjects both ingested a breakfast 3 h before and 30 g of glucose 15 min before the beginning of exercise.

In conclusion, results from the two studies available in the literature (11, 24) and results from the present experiment suggest that, compared with control subjects, when exogenous glucose is ingested immediately before or during exercise in diabetic patients, although its availability could be slightly delayed, its oxidation rate is not significantly reduced. Moreover, these results suggest that, when glucose is ingested before exercise, diabetic patients rely more on muscle glycogen and less on plasma glucose oxidation than control subjects.

	GRANTS

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This study was supported by the Canadian Diabetes Association and the Natural Sciences and Engineering Research Council of Canada.

	ACKNOWLEDGMENTS

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The authors are grateful to Claire Chénard and Alexandre Melançon (Laboratoire de biochimie de l'exercice, Université du Québec à Trois-Rivières) and Jennifer McKay (GEOTOP, Université du Québec à Montréal) for technical assistance.

	FOOTNOTES

 

Address for reprint requests and other correspondence: Carole Lavoie, Département des sciences de l'activité physique, Université du Québec à Trois-Rivières, Case postale 500, Trois-Rivières, Québec, Canada G9A 5H7 (e-mail: Carole.Lavoie{at}uqtr.ca)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

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