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1 Children's Exercise and Nutrition Centre, 2 Department of Medicine, and 3 School of Geography and Geology, McMaster University, Hamilton, Ontario, Canada L8N 3Z5
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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This study was intended to compare exogenous [13C]glucose (Gluexo) oxidation in boys with insulin-dependent diabetes mellitus (IDDM) and healthy boys of similar age, weight, and maximal O2 uptake. In a control trial with water intake (CT) and in a 13C-enriched glucose trial (GT), subjects cycled for 60 min (58.8 ± 0.9% maximal O2 uptake) while the utilization of total glucose, total fat, and Gluexo was assessed. In CT, total glucose was 84.7 ± 9.2 vs. 91.3 ± 6.6 g/60 min (not significantly different) and total fat was 13.3 ± 2.2 vs. 11.1 ± 1.7 g/60 min (not significantly different) in IDDM vs. healthy boys, respectively. In GT, Gluexo was 10.4 ± 1.7 vs. 14.8 ± 1.1 g/60 min, corresponding to 9.0 ± 1.0 vs. 12.4 ± 0.5% of the total energy supply in IDDM and healthy boys, respectively (P < 0.05). Endogenous glucose was spared in both groups by 12.6 ± 3.5% (P < 0.05). Blood glucose and plasma insulin concentrations were two- to threefold higher in IDDM vs. healthy boys in both trials. In conclusion, Gluexo is impaired in exercising boys with IDDM, even when plasma insulin levels are elevated.
adolescents; carbohydrates; insulin; blood glucose; insulin-dependent diabetes mellitus
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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EXOGENOUS GLUCOSE (Gluexo) postpones
fatigue during prolonged, moderate-intensity exercise both in healthy
adults (12) and in adults with insulin-dependent diabetes mellitus
(IDDM) (31). Gluexo ingestion is thought to limit fatigue
by elevating blood glucose concentrations ([glucose]) and
by maintaining high rates of glucose oxidation late in exercise (10).
Gluexo oxidation during exercise in healthy male subjects
has been investigated intensively by using stable
[13C]glucose tracers (for review see Ref. 27);
however, only one study (21) has examined Gluexo oxidation
in individuals with IDDM. In that experiment, Krzentowski et al. (21)
showed that Gluexo oxidation in intravenously
insulin-infused, euglycemic men with IDDM was similar to that in
controls but was reduced by 50% when the insulin was withheld. Hawley
and colleagues (19) and, more recently, Weltan et al. (37) have shown
that, at least in healthy nondiabetic individuals, experimentally
induced hyperinsulinemia and hyperglycemia increase glucose oxidation
during exercise. Despite the above evidence indicating that
Gluexo oxidation may be increased by high plasma insulin
concentrations ([insulin]), no studies exist that examine
Gluexo oxidation during exercise performed after
subcutaneous insulin injection in individuals with IDDM. Indeed,
individuals with IDDM often perform spontaneous physical activities
1-2 h after insulin injection, causing elevations in circulating
plasma [insulin] compared with nondiabetic individuals (41). To combat hypoglycemia, caused by relative hyperinsulinemia, these individuals are often advised to consume additional carbohydrates either before or during exercise (1). It is possible, therefore, that
Gluexo oxidation may be elevated in individuals with IDDM who exercise after subcutaneous insulin injection, compared with their
nondiabetic peers. No studies exist to test this hypothesis, however.
We therefore compared Gluexo oxidation during prolonged, moderate-intensity exercise performed after insulin injection in boys
with IDDM and in healthy nondiabetic boys of similar age, weight, and
maximal O2 uptake
(
O2 max).
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects.
Eight 13- to 19-yr-old boys with IDDM and six healthy nondiabetic boys
of similar age, weight, and
O2 max volunteered in response to local public service announcements. Their physical and
functional characteristics are shown in Table
1. Volunteers with IDDM were
eligible for the study if they had no residual 
-cell function, as
indicated by a postmeal plasma C-peptide level of <0.03 nmol/l. All
IDDM subjects took two insulin injections per day and were nonobese,
habitually active, but not competitive athletes. They were considered
to be in fair to poor control of their diabetes during the study period
(40) (on the basis of glycosylated hemoglobin ranging from 9 to 15%,
normal range from 4 to 7%) and had no evidence of retinopathy,
autonomic neuropathy, or nephropathy, as assessed by their physician.
The purpose, nature, and possible risks of the experiment were
explained to the subjects and their parents. Subjects 14 yr or older
and their parents signed informed consent. Those under 14 yr of age
gave a verbal assent, and a parent then signed an informed consent. The
study was approved by the Research Ethics Board of the Faculty of
Health Sciences, McMaster University.
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Preliminary session.
At least 1 wk before the first experimental trial, height, weight, and
percent body fat (1990B Bio-resistance Body Composition Analyzer,
Valhalla Scientific) were measured, and 3-day dietary intake forms were
provided for dietary assessment.
O2 max was determined
during progressive cycle ergometry, each stage lasting 2 min (3).
Measurements of (O2) and
CO2 production
(CO2) were made
continuously by using a Quinton metabolic cart (Quinton Q-plex 1, Quinton Instrument, Seattle, WA) and averaged over the final 30 s of
each stage. Heart rate was measured throughout the test by using a
Sports Tester PE3000 system (Polar Electro, Kempele, Finland).
Experimental trials.
Two experimental trials [control trial (CT) followed by a glucose
trial (GT)] were spaced 1-4 wk apart. Subjects were asked to
maintain a similar diet, exercise, and insulin routine (IDDM group) the
day before each experimental session. The two trials were identical
except for carbohydrate intake before and during exercise. After the
subjects arrived at the laboratory on the mornings of the trials
(0800), capillary blood was sampled from a finger at 100 min before the
start of exercise (time = 
100 min) and analyzed for fasting
capillary blood glucose by using an Accu-Check IIIm glucose monitor
(Boehringer Mannheim, Laval, PQ). This meter was shown to have a high
correlation to blood glucose assay measurements on the basis of data
pairs from blood drawn in our laboratory (r = 0.97, y = ax + b, where y is hexokinase assay, a = 1.00, b = 0.39, and SE of estimate = 1.53; n = 141). Subjects
with IDDM then injected their usual morning insulin dose into their
left arm (7 ± 2 IU regular insulin and 25 ± 3 IU long-acting insulin). No adjustment in insulin dose was made in anticipation of
exercise. An individualized breakfast was provided by the investigators that matched for percent carbohydrate, protein, and fat composition on
the basis of the 3-day dietary intake forms filled out by the subjects.
The meal provided 2,201 ± 854 (SD) kJ of total energy (~65%
carbohydrate, ~15% protein, and ~20% fat). Foods naturally enriched in [13C]carbohydrate (i.e., corn and
food items derived from corn) were avoided to limit baseline shifts in
expired 13CO2. After breakfast, an indwelling
catheter was inserted into a forearm vein from which blood was
collected into heparinized syringes intermittently throughout the
trials. One portion of the sample was deproteinized in 2 vol of 6%
perchloric acid, stored at 20°C, and subsequently analyzed
for blood [glucose], lactate concentration
([lactate]), and glycerol concentration
([glycerol]) by using standard fluorometric techniques (6).
A second portion was centrifuged at 15,900 g for 2 min, and the
plasma supernatant was stored at 20°C and subsequently
analyzed for free fatty acid concentration ([FFA];
enzymatic colorimetric technique, Wako NEFA C kit, Wako Chemicals,
Dallas, TX) and [insulin] (Coat-A-Count radioimmunoassay,
DPC Diagnostics). In addition, the Accu-Check glucose meter was used to
measure all venous samples for [glucose] as a safety
measure in case of hypoglycemia, especially in the subjects with IDDM.
Exercise on a cycle ergometer began 80-90 min after the start of
breakfast and consisted of two 30-min bouts, separated by a 5-min rest.
The rest period was provided to limit boredom and to allow the subjects
to empty their bladder. During both trials, subjects exercised at an
intensity corresponding to 58.8 ± 0.9% of their predetermined
O2 max. During the
CT, they were given water intermittently as fluid replenishment in quantities individualized to maintain euhydration (ranging from 625 to
1,000 ml/h exercise). In the GT, subjects consumed five equal amounts
of Gluexo beverage at 20, 5, 15, 30, and 50 min (time = 0 min denotes the start of the first exercise bout). The amount of Gluexo consumed in the entire GT was equal to the
total glucose (Glutot) oxidized in the CT. This
Gluexo feeding pattern was chosen because it attenuates the
drop in [glucose] and reduces the likelihood of
hypoglycemia in adolescents with IDDM (33). The Gluexo was
provided in an 18 mmol/l NaCl, grape-flavored solution (8%
D-glucose). The D-glucose in the beverage was
derived from corn (BDH-Chemical, Toronto, ON) and artificially enriched
with uniformly labeled [13C]glucose (99 atom
%excess, Isotec, Miamisburg, OH) to an isotopic composition of +16.3
change per 1,000 difference vs. the 13C/12C
ratio from the international standard 13C Pee Dee
Belemnitella-1 (PDB-1; +16.3
[
13C]PDB-1). This high
level of enrichment, compared with that of normal expired gas
(22.4 [13C]PDB-1 in this
study), provides a strong measurement signal and reduces the error
associated with the small shift in the isotopic composition of
CO2 arising from the oxidation of endogenous substrates during exercise (23).
Respiratory gas and substrate oxidation.
Resting O2 and
CO2 were
determined with subjects sitting quietly in a chair during a 5-min
collection period at 25 min. In addition,
O2 and
CO2 were determined during
exercise from 3-min sampling periods at 10, 25, 40, and 60 min. Expired
gas concentrations were validated periodically during each trial
against CO2, O2, and N2 gas mass
spectrometry (Perkin-Elmer AeroSpace Systems, Pomona, CA).
Glutot and total fat (Fattot) oxidation rates
were calculated at each time point from respiratory exchange ratio
(RER) and O2 averaged over
the collection period by using a table of nonprotein respiratory
quotients (28). During gas sampling in the GT, duplicate 20-ml expired
gas samples were drawn from Douglas bags connected to the exhaust port
of the metabolic cart and stored in vacutainer tubes for subsequent
determination of 13C/12C in expired
CO2 and Gluexo oxidation. In these tubes, water
vapor and CO2 were separated from other gases by a liquid
nitrogen trap (196°C). CO2 was then separated
from water vapor by using an acetone-dry ice slush trap
(80°C). The isotopic composition of the CO2 was
then determined by using a dual-inlet mass spectrometer (VG-Sira 10, series II, Manchester, UK) and expressed in
[13C]PDB-1. Gluexo
oxidation was calculated for the sampling periods by using the formula
of Mosora et al. (26)
](/content/vol88/issue4/fulltext/1239/img001.gif)
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CO2 is in liters per minute
STPD, Rexp is the isotopic composition of
expired CO2 during exercise, Rref is the
isotopic composition of expired CO2 at rest before
Gluexo ingestion, Rexo is the isotopic
composition of the Gluexo, and k (0.7426 l/g) is
the volume of CO2 provided by the complete oxidation of
glucose (28). This method of determining Gluexo oxidation
assumes that 13CO2 recovery in expired gas
during exercise is complete or almost complete (22). Endogenous glucose
(Gluendo) oxidation was calculated by subtracting
Gluexo from total carbohydrate oxidation.
Statistical analyses. Data are presented as means ± SE. For measurements taken repeatedly during both trials and in both groups, a three-way mixed-design ANOVA was used. Tukey's honest significant difference post hoc test for unequal cell size was used to determine significance among mean values. Intergroup differences in physical and functional characteristics were compared by using a nonpaired t-test.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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All subjects successfully completed the two 30-min exercise bouts and consumed the provided beverages in the allotted time periods. The average volume of Gluexo beverage consumed at each of the five drink periods in the GT was 213 ± 23 and 228 ± 17 ml (corresponding to 17.0 ± 1.8 and 18.2 ± 1.3 g glucose) for IDDM and healthy boys, respectively.
RER, heart rate, O2, and
substrates.
RER at rest before beverage intake was similar between trials but was
lower in the IDDM group (0.83 ± 0.01) vs. healthy group (0.89 ± 0.01; P < 0.05). During exercise, mean heart rate,
O2, and RER were similar for
groups, trials, and time points (Table 2).
The work rate was also similar among the groups, trials, and time
points, averaging 90 ± 8 W.
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Blood variables.
Blood [glucose] in the healthy boys was similar in both
trials at fasting (100 min) and before beverage intake
(20 min), averaging 5.0 ± 0.1 mmol/l (Fig.
3). In the CT, [glucose]
remained relatively stable in the healthy group but was somewhat
elevated (+1-2 mmol/l; P < 0.05) after beverage intake
in the GT. In the IDDM group, [glucose] was, on average,
higher than in the healthy group (P < 0.01). Levels were
similar in both trials before beverage intake, increasing from 8.0 ± 1.2 at fasting to 14.9 ± 1.3 mmol/l (P < 0.001) by
20 min. In the CT, [glucose] decreased throughout exercise from 15.0 ± 2.0 at 5 min to 6.9 ± 1.5 mmol/l at 65 min (P < 0.001), with four subjects experiencing levels below
4.0 mmol/l by the end of exercise. During the GT, [glucose]
was significantly higher than in the CT at all time points during
exercise but also decreased from 16.3 ± 2.1 at 5 min to 11.7 ± 1.6 mmol/l by 65 min (P < 0.01) with no subjects
experiencing levels below 4.0 mmol/l.
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5 min to 11.2 ± 2.8 µIU/ml at 65 min (P < 0.05; Fig.
4). In the GT, [insulin]
decreased from 60.7 ± 12.3 at 5 min to 27.0 ± 8.2 µIU/ml
(P < 0.01) but was significantly higher than in the CT at 30 (P < 0.05) and 65 min (P < 0.05). In the IDDM
group, [insulin] was approximately twofold higher than in
the healthy group (P < 0.05) but was similar in both trials
and at all time points, averaging 112.5 ± 13.4 µIU/ml.
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5 min to 0.50 ± 0.09 mmol/l by
65 min (P < 0.05) in the CT but remained relatively stable in the GT.
In the IDDM group, [FFA] at rest before beverage intake was
also similar between trials but was significantly higher than in the
healthy group (P < 0.05), averaging 0.48 ± 0.05 mmol/l
(Fig. 5). During exercise, [FFA] decreased in both trials
in the IDDM group from 0.47 ± 0.04 at 5 min to 0.28 ± 0.02 mmol/l by 65 min (P < 0.05).
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5 min to 0.08 ± 0.010 mmol/l at 65 min (P < 0.05) in the CT but remained unchanged significantly in the GT. In the
IDDM group, [glycerol] was similar in both trials and
unchanged during exercise, averaging 0.034 ± 0.001 mmol/l.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The main finding of this study is that, despite higher circulating [insulin] (Fig. 4), Gluexo oxidation during 60 min of moderate-intensity exercise in adolescent boys with IDDM is lower than in healthy age- and weight-matched controls (Figs. 1 and 2). This finding is similar to the results of Krzentowski et al. (21), who found that Gluexo oxidation was somewhat impaired during prolonged exercise in adult men with IDDM compared with healthy controls. The IDDM subjects in that study, however, were treated with a low basal rate of intravenous insulin infusion and were fasted during the exercise. In our study, subjects injected insulin subcutaneously and ingested a preexercise meal before exercise. Our protocol was designed to examine Gluexo oxidation during exercise in adolescents with IDDM during their usual insulin and diet therapy when [glucose] and [insulin] are elevated in comparison to their nondiabetic peers. Because hyperinsulinemia and hyperglycemia increase glucose oxidation in healthy nondiabetic subjects (19, 37), we hypothesized that Gluexo oxidation would be higher in the subjects with IDDM compared with healthy controls. However, although our subjects with IDDM were exercising with high [glucose] (Fig. 3) and [insulin] (Fig. 4), Gluexo oxidation was lower at all time points than in healthy controls (Fig. 1).
Because the 13CO2 production at the mouth may lag behind the actual Gluexo oxidation rate as a result of the presence of the large bicarbonate pool (9), we have also reported substrate utilization during the second exercise bout separately (Table 3). No differences in substrate utilization were found during the second exercise bout between groups, although there was a tendency for Gluexo oxidation to be lower in the IDDM group (P = 0.20). The failure to show a quantitative difference in substrate utilization during the second bout between the IDDM and healthy groups may have resulted from our relatively small sample size (n = 8 vs. n = 6, respectively). Nevertheless, although an exact quantitative assessment of Gluexo oxidation may not have been reached during the initial 30-min exercise in our study, we assume that the 13C/12C equilibrium kinetics are similar in IDDM and healthy adolescents and that any small error in determining Gluexo oxidation should be equal for both groups. We believe, therefore, that from the qualitative assessment of Gluexo oxidation (Figs. 1 and 2), it appears that Gluexo oxidation in IDDM is impaired. This finding not only causes us to reject our initial hypothesis that hyperinsulinemia would enhance Gluexo oxidation in IDDM but also further indicates that Gluexo oxidation is impaired even during exercise performed after subcutaneous insulin injection.
Previous studies have shown that glucose uptake and utilization are clearly impaired in animal models of IDDM when insulin is absent or reduced (5, 38). In addition, in insulin-deprived IDDM human subjects, Gluexo oxidation is impaired by ~50% compared with controls (21). There are contrasting data, however, regarding the influence of normalizing insulin levels on glucose utilization during exercise in patients with IDDM. Plasma glucose utilization has been reported to be both similar (35) or significantly reduced (30) when compared with that of nondiabetic subjects exercising at the same [insulin]. In support of the latter, plasma glucose uptake has been shown to be restored to normal only if [insulin] is approximately fourfold higher in IDDM compared with healthy individuals (41). In line with these findings of impaired glucose uptake in insulin-treated IDDM, our study shows that orally ingested Gluexo oxidation is lower in IDDM compared with healthy controls, despite [insulin] values that are threefold higher.
The reduced Gluexo oxidation in the subjects with IDDM may
be explained by several possible factors. First, a lower rate of gastrointestinal absorption of glucose may have limited
Gluexo oxidation during exercise. Delays in gastric
emptying time and gastric electrical abnormalities at rest have been
associated with poor glycemic control in children with IDDM (13).
Furthermore, hyperglycemia impedes gastric emptying in IDDM (34), and
experimental hyperinsulinemia reduces carbohydrate absorption at least
in healthy individuals (15). Although we did not measure plasma glucose enrichment in our subjects to assess glucose absorption, our subjects with IDDM who were both hyperglycemic and hyperinsulinemic would be
expected to have impaired Gluexo absorption. These
potential impairments in glucose absorption in our subjects may have
resulted in a lower Gluexo oxidation. Second, it appears
from the elevated glycemic (Fig. 3) and insulin (Fig. 4) concentrations
that our subjects with IDDM have some degree of insulin resistance that may limit plasma glucose uptake and oxidation. Indeed, adolescents with
IDDM are especially prone to insulin resistance and poor diabetes
management (2). A reduction in skeletal muscle glucose-transporter density (specifically the GLUT-4 isoform) has been associated with
insulin resistance in IDDM (20). A lower density of GLUT-4 isoform or
an inability to activate the transporter mechanism (29) may reduce
Gluexo uptake and oxidation in IDDM even if [insulin] values are elevated. Interestingly, however, no
relationships between either individual glycosylated hemoglobin levels
(r = 0.10) or [insulin] (r =
0.12) and Gluexo oxidation were found. Because we
did not measure plasma glucose uptake in our study, we are unsure
whether a lower Gluexo oxidation was a result of a reduced
skeletal muscle uptake of glucose. Third, Gluexo oxidation may be impaired in insulin-treated individuals with IDDM because of an
impairment in a key regulatory enzyme of glucose oxidation [i.e.,
pyruvate dehydrogenase (PDH) complex]. In healthy adults, the
oxidation of ingested carbohydrate may be regulated by the activation
of the PDH complex (36) and an impairment in this activation (16) may
reduce Gluexo oxidation in IDDM. Although we did not
measure PDH activity directly in this study, the elevated [FFA] observed at rest in the subjects with IDDM would be
expected to inactivate the PDH complex, according to the glucose-fatty acid cycle as proposed by Randle et al. (32). Indeed, elevations in
[FFA] associated with diabetes appear to lower skeletal
muscle glucose uptake and oxidation (4). Conceivably, these potential impairments in gastrointestinal glucose absorption, insulin
sensitivity, skeletal muscle glucose transport, and PDH activation may
help to explain the reduction in Gluexo oxidation in our
subjects with IDDM.
In addition to the lower rate of Gluexo oxidation compared with controls, our subjects with IDDM tended to utilize less total carbohydrate and more fat both at rest and during exercise (Table 3). This finding is in agreement with a recent study examining substrate utilization during moderate and intense exercise in adults with IDDM (30). In our study, the difference in Glutot and Fattot oxidation during exercise between IDDM and healthy boys was not statistically significant, however, possibly because of our small sample sizes. Interestingly, although [insulin] was elevated compared with controls, [FFA] was also somewhat elevated (Fig. 5). The elevated [FFA], along with lower RER during rest and exercise in IDDM, indicates a greater reliance on fat oxidation compared with that in the healthy boys. Furthermore, it appears that individuals with IDDM lack the expected increase in [glycerol] and [FFA] normally observed with prolonged exercise without carbohydrate intake (Fig. 5). These findings indicate that substrate utilization and the metabolic response to exercise are not restored to normal with subcutaneous insulin administration.
The use of [13C]glucose tracer allows for an indirect estimation of Gluendo during exercise. In this study, Gluendo was lower in the GT compared with the CT (Fig. 2, Table 3), indicating that Gluexo ingestion spares endogenous glycogen stores by ~12% in adolescents with and without IDDM. A similar Gluendo sparing effect with Gluexo intake has also been shown in healthy adults (24). In line with these findings, glucose intake appears to reduce hepatic glucose output (25) and may lower muscle glycogen utilization if the dose of glucose is large enough or if the exercise is of an intermittent type (8, 18, 39). However, other investigations have found no muscle glycogen-sparing effect with Gluexo intake (7, 11, 17). Because of methodological limitations in this study, we are unsure what source of Gluendo was spared with Gluexo intake.
Blood [glucose] in the individuals with IDDM decreased significantly during exercise with water ingestion, but this drop was attenuated with Gluexo ingestion (Fig. 3). The attenuation of the hypoglycemic effect of exercise with Gluexo intake matched with Glutot has been reported by us previously (33). In contrast to the subjects with IDDM, [glucose] in the healthy boys did not change significantly during exercise with water ingestion but was slightly elevated with Gluexo intake. A small decrease in glycemia has been reported after the onset of postprandial exercise in healthy 8- to 11-yr-old boys and girls (14).
In conclusion, the oxidation rate of exogenous glucose during prolonged moderate-intensity exercise is impaired in boys with IDDM compared with healthy nondiabetic boys even though plasma insulin levels are elevated after subcutaneous insulin injection in these patients. Gluexo ingestion matched with Glutot utilization contributes from 9 to 12% of the total energy provision of exercise in adolescent boys with and without IDDM and is effective in attenuating the drop in blood glucose in boys with IDDM.
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ACKNOWLEDGEMENTS |
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We thank M. Knyf for technical assistance in measuring 13C/12C of CO2 in expired gas samples and Dr. F. Péronnet and colleagues at the University of Montreal for assistance in the methods for determining Gluexo oxidation.
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FOOTNOTES |
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This work was supported by the Gatorade Sports Science Institute, the Medical Research Council of Canada, and the Natural Science and Engineering Council of Canada.
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. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: O. Bar-Or, Children's Exercise and Nutrition Centre, McMaster Univ., Chedoke Hospital Div., Evel Bldg., 4th Fl., PO Box 2000, Hamilton, ON, Canada L8N 3Z5 (E-mail: baror{at}fhs.mcmaster.ca).
Received 5 March 1999; accepted in final form 23 November 1999.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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