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Am J Physiol Endocrinol Metab 292: E865-E870, 2007; doi:10.1152/ajpendo.00533.2006 Free Article
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Effect of intermittent high-intensity compared with continuous moderate exercise on glucose production and utilization in individuals with type 1 diabetes

K. J. Guelfi,1 N. Ratnam,2,3 G. A. Smythe,4 T. W. Jones,2,3 and P. A. Fournier1

1School of Human Movement and Exercise Science, University of Western Australia, Crawley; 2Department of Endocrinology and Diabetes, Princess Margaret Hospital, Subiaco; 3Centre for Child Health Research, The University of Western Australia, Telethon Institute of Child Health Research, Perth, Western Australia; and 4Bioanalytical Mass Spectrometry Facility, School of Medical Sciences, University of New South Wales, Sydney, New South Wales, Australia

Submitted 29 September 2006 ; accepted in final form 10 November 2006


   ABSTRACT
TOP
 ABSTRACT
EXPERIMENTAL PROCEDURES
 RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Previously, the decline in glycemia in individuals with type 1 diabetes has been shown to be less with intermittent high-intensity exercise (IHE) compared with continuous moderate-intensity exercise (MOD) despite the performance of a greater amount of total work. The purpose of the present study was to determine whether this lesser decline in glycemia can be attributed to a greater increment in endogenous glucose production (Ra) or attenuated glucose utilization (Rd). Nine individuals with type 1 diabetes were tested on two separate occasions, during which either a 30-min MOD or IHE protocol was performed under conditions of a euglycemic clamp in combination with the infusion of [6,6-2H]glucose. MOD consisted of continuous cycling at 40% VO2 peak, whereas IHE involved a combination of continuous exercise at 40% VO2 peak interspersed with additional 4-s maximal sprint efforts performed every 2 min to simulate the activity patterns of intermittent sports. During IHE, glucose Ra increased earlier and to a greater extent compared with MOD. Similarly, glucose Rd increased sooner during IHE, but the increase by the end of exercise was comparable with that elicited by MOD. During early recovery from IHE, Rd rapidly declined, whereas it remained elevated after MOD, a finding consistent with a lower glucose infusion rate during early recovery from IHE compared with MOD (P < 0.05). The results suggest that the lesser decline in glycemia with IHE may be attributed to a greater increment in Ra during exercise and attenuated Rd during exercise and early recovery.

glycemia; hypoglycemia; physical activity

FOR INDIVIDUALS WITH TYPE 1 DIABETES, participation in exercise generally increases the risk of experiencing hypoglycemia both during exercise (31, 36) and for up to 31 h of recovery (22). Consequently, these individuals may fear or be discouraged from physical activity (13) despite the well-established benefits of exercise (18, 27, 28). Although hypoglycemia is a legitimate fear, the American Diabetes Association Position Statement on Physical Activity/Exercise and Diabetes (43) states that complication-free individuals with type 1 diabetes can safely enjoy the benefits of physical activity by balancing exogenous insulin administration and carbohydrate intake to maintain glucose levels within the euglycemic range. However, effective adjustment of these parameters requires an understanding of the metabolic and hormonal responses to exercise (43). For this reason, much research has focused on investigating the glucoregulatory responses to exercise.

It is well established that continuous exercise of moderate-intensity causes a decline in blood glucose levels (31, 36), whereas sustained high-intensity exercise [~15 min at >80% maximal oxygen uptake (VO2 max)] stimulates a progressive rise in glycemia during exercise and prolonged hyperglycemia during recovery (30, 34). On the other hand, the response of blood glucose levels to a combination of moderate and high-intensity exercise, a pattern of physical activity referred to as intermittent high-intensity exercise (IHE), is less well understood. IHE involves repeated bouts of short, intense activity, interrupting longer periods of lower-intensity activity or rest. This type of exercise characterizes most team and field sports and accounts for much of the selection of activities participated in by individuals with type 1 diabetes (32), as well as spontaneous play in children (1).

Recently, the glucoregulatory responses to IHE that reflect the work-to-recovery ratios observed in team and field sports have been compared with continuous moderate-intensity exercise (MOD) (15). The experimental design simulated a "real-life" situation in which the participants injected their normal morning dose of insulin and consumed their typical breakfast prior to the performance of exercise ~3.5 h later. It was found that the decline in glycemia was less with IHE compared with MOD both during exercise and throughout the first hour of recovery. This was despite the performance of a greater amount of total work with IHE. The authors hypothesized that the lesser decline in glycemia with IHE may have resulted from a greater increase in hepatic glucose production and attenuated glucose utilization. Since this issue has not previously been addressed, the purpose of the present study was to compare the effect of IHE and MOD on the rate of glucose production and utilization during and after exercise in individuals with type 1 diabetes.


   EXPERIMENTAL PROCEDURES
TOP
 ABSTRACT
 EXPERIMENTAL PROCEDURES
RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Participants. Nine healthy, physically active male (n = 5) and female (n = 4) volunteers with type 1 diabetes [age 22.6 ± 5.7 yr, body mass index (BMI) 24.6 ± 2.2 kg/m2, peak oxygen uptake (VO2 peak) 41.8 ± 4.6 ml·kg–1·min–1, duration of type 1 diabetes 5.6 ± 3.9 yr (mean ± SD)] were informed of the purpose of the study and the possible risks associated with exercise and blood sampling. These individuals gave informed consent in accordance with the Princess Margaret Hospital Human Ethics Committee, which approved the study. Six of the participants were on a multiple-injection regimen, and three were treated with a subcutaneous insulin infusion pump. All participants were in moderate glycemic control (Hb A1c 7.7 ± 0.8%), free of complications, and not taking any prescribed medication other than insulin, and females were regularly menstruating.

Experimental design The participants visited the laboratory on three occasions, each separated by at least 1 wk. The first visit involved a familiarization session, during which anthropometric measurements, determination of VO2 peak, and familiarization with the IHE and MOD protocols were performed. This initial visit was followed by either a MOD or IHE trial administered in a randomized, counterbalanced order. Participants were instructed to consume a similar diet for both trials and avoid caffeine, alcohol, and physical activity during the 24 h prior to testing. In addition, testing was rescheduled if a participant experienced an episode of hypoglycemia in the 48 h prior. All female participants were tested during the follicular phase of the menstrual cycle (day 8 ± 3), with ~4 wk between trials.

On MOD and IHE trials, participants arrived at the laboratory by 0730 in an overnight-fasted state. On arrival, a cannula was inserted retrogradely into a superficial dorsal hand vein for blood sampling. This hand was warmed in a HotBox (Omega CN370) at ~60°C for the sampling of arterialized venous blood. A second cannula was inserted into an antecubital vein on the contralateral arm to allow for the infusion of insulin, dextrose, and [6,6-2H]glucose. Next, a constant infusion of 20 mU·m2·min–1 of insulin (Humalog; Eli Lilly Australia) was commenced. This rate of insulin infusion was selected to reproduce the initial levels of circulating insulin in our previous study (13). Blood glucose levels were maintained at ~5.5 mmol/l for the duration of the experiment by infusing 20% dextrose solution at a variable rate determined via manual feedback from the blood glucose level measured in arterialized venous blood at 15-min intervals.

After the commencement of the insulin infusion, a blood sample was drawn for determination of background enrichment, and the infusion of [6,6-2H]glucose (Cambridge Isotope Laboratories, Andover, MA) was initiated (n = 8) with a priming bolus of 3 mg/kg and a constant infusion of 2.4 mg·kg–1·h–1 that was continued for the duration of the experiment. In addition, the variable infusion of dextrose to maintain euglycemia was "spiked" with [6,6-2H]glucose (2.48 mg/ml) to minimize changes in the isotopic enrichment of plasma glucose in response to adjustments in the glucose infusion rate (11). For the next 150 min the participant remained rested in a seated position to allow for isotope equilibration, with stable enrichment confirmed via blood sampling in the final 30 min of this period. While they rested, expired air was collected from each participant via a mask connected to a Vmax Spectra respiratory analysis system (SensorMedics) for at least 10 min for the determination of baseline rates of O2 consumption and CO2 production.

After this equilibration period, blood was sampled for baseline measurements and the participant moved to an adjacent Front Access Cycle ergometer (Repco). The rate of constant isotope infusion was doubled to attenuate changes in isotopic enrichment during exercise (8, 30), and the participant commenced either 30 min of MOD or IHE. The MOD protocol consisted of 30 min of continuous cycling at 40% VO2 peak to simulate the intensity of a light jog. The IHE protocol also involved continuous cycling at 40% VO2 peak, but this was interspersed with additional 4-s maximal sprint efforts performed every 2 min to simulate the high-intensity work-to-recovery ratios observed in intermittent sports (16, 21, 41) and spontaneous play in children (1). Although tracer methodology is not typically applied to the type of IHE examined in this study, it has been used previously to investigate glucose kinetics during intermittent exercise involving longer (4 min), high-intensity bouts (19) and has been used extensively to examine other non-steady-state exercise protocols of sustained high intensity (30, 34).

During exercise, blood was sampled every 5 min and expired air collected for the determination of the rate of O2 consumption and CO2 production. At the completion of exercise, the isotope infusion was returned to the preexercise rate and maintained until 2 h postexercise, during which time blood continued to be regularly sampled. Expired air was also collected at 60 and 120 min of recovery. On completion of the experiment, each participant was fed and allowed to leave the laboratory if blood glucose levels were >5 mmol/l.

Measurement of hormones and metabolites. Blood samples were analyzed for glucose and lactate levels using a YSI glucose and lactate analyzer (YSI Life Sciences, Yellow Springs, OH), whereas isotopic enrichment was determined via gas chromatography-mass spectrometry (GC-MS) (Agilent Technologies 6890 gas chromatograph interfaced to an Agilent 5973 Mass Selective Detector; Agilent Technologies, Ryde, NSW, Australia). The remaining blood was assayed for free insulin, free fatty acids (FFAs), glucagon, growth hormone, and cortisol levels using methods previously described (15). Catecholamine levels were determined on heparinized plasma treated with sodium metabisulphite using a BI-CAT ELISA kit (Diagnostika, Germany).

Calculations. Isotopic enrichment determined by GC-MS was corrected for the constant background contribution of naturally occurring [6,6-2H]glucose, and the values obtained were smoothed using a spline-fitting procedure to minimize random error of measurement (10). The rates of endogenous glucose production (Ra) and glucose utilization (Rd) were estimated using Steele's one-compartment fixed-volume model (35), as modified by Finegood et al. (11), to account for the added infusion of exogenous glucose. A volume of distribution of 100 ml/kg was used for the calculations.

Statistical analyses. Data were analyzed using SPSS 11.0 for Windows computer software package. Measures of each variable were subjected to two-way (time x trial) repeated-measures analysis of variance to determine whether differences existed, followed by paired t-tests to determine where the differences lay. Baseline data used for glucose infusion rate (GIR), Ra, and Rd were the mean levels over the 30 min prior to exercise. Statistical significance was accepted at the P < 0.05 level. Data are expressed as means ± SD when referred to in the text and as means ± SE in all figures.


   RESULTS
TOP
 ABSTRACT
 EXPERIMENTAL PROCEDURES
 RESULTS
DISCUSSION
 GRANTS
 REFERENCES
 
Euglycemic clamp. Blood glucose levels were maintained at ~5.5 mmol/l, with no difference between trials (Fig. 1A). The constant infusion of insulin resulted in free insulin levels of 154 ± 64 vs. 165 ± 63 pmol/l at the commencement of MOD and IHE, respectively. These levels increased during exercise but remained stable during recovery, with no difference between trials at any time (Fig. 1B). The GIR required to maintain euglycemia was similar between trials at baseline and increased during both exercise protocols (Fig. 1C). Although the pattern of response of GIR appeared to be different during the two types of exercise, there was no statistical difference between trials. During early recovery, GIR remained elevated following both protocols but was significantly higher after MOD compared with IHE at 5 min of recovery (P = 0.049). During later recovery from MOD, GIR returned to baseline but remained slightly elevated after IHE, although there was no difference between trials.


Figure 1
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  		Fig. 1. Effect of 30 min (represented by box) of moderate-intensity exercise (MOD; {circ}) or intermittent high-intensity exercise (IHE; bullet) on blood glucose (A), free insulin (B), and the glucose infusion rate (GIR) required to maintain euglycemia (C). Results are expressed as means ± SE. a Statistically significant difference (P < 0.05) between MOD and IHE; b statistically significant difference (P < 0.05) from preexercise.

 
Glucose Ra and Rd. Isotopic enrichment was stable prior to the commencement of exercise and remained relatively constant for the duration of the experiment (coefficient of variation = 7.8%). With the onset of exercise, endogenous Ra progressively increased to peak at the cessation of exercise (Fig. 2A). However, the rise in Ra commenced sooner and was of a greater magnitude during IHE compared with MOD, with the latter difference reaching statistical significance at 15 min of exercise (P = 0.05). Postexercise, Ra rapidly declined but remained above baseline levels for the first hour of recovery. During the second hour of recovery, Ra returned to baseline with MOD but remained slightly elevated after IHE. Basal glucose Rd was equivalent in both trials and progressively increased during exercise to a similar extent; however, the rise commenced earlier during IHE (Fig. 2B). Immediately postexercise, Rd declined to baseline with IHE, whereas it remained elevated after MOD. During later recovery from IHE, Rd rose again above baseline, whereas after MOD Rd remained at baseline from 30 min. At 2 h postexercise, Rd was significantly higher after IHE compared with MOD (P = 0.045).


Figure 2
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  		Fig. 2. Effect of 30 min (represented by box) of MOD ({circ}) or IHE (bullet) on rate of endogenous glucose production (Ra; A) and rate of glucose utilization (Rd; B). Results are expressed as means ± SE. a Statistically significant difference (P < 0.05) between MOD and IHE; b statistically significant difference (P < 0.05) from preexercise.

 
Total work, heart rate, and oxygen consumption. A greater amount of total work was performed during IHE compared with MOD (2,882 ± 385 vs. 2,199 ± 289 J/kg, P = 0.000). This greater amount of total work was reflected by the response of heart rate and oxygen consumption to exercise, which increased to a greater extent during IHE (Table 1). The higher average rate of oxygen consumption during IHE corresponded to ~55% of VO2 peak compared with 40% during MOD.


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  		Table 1. Effect of MOD and IHE on heart rate and VO2

 
Metabolites and hormones. Blood lactate increased during both exercise protocols, but the increase was greater with IHE compared with MOD (P = 0.000; Fig. 3A). In contrast, the levels of circulating FFAs were not different between MOD and IHE, remaining stable during exercise but increasing after 2 h of recovery (Fig. 3B). Epinephrine levels were not significantly increased in response to MOD or IHE, and there was no difference between protocols (Fig. 3C). On the other hand, norepinephrine increased during both exercise protocols, with a greater increase in response to IHE compared with MOD (P = 0.012; Fig. 3D). Growth hormone levels also rose during IHE, remaining elevated for the first 15 min of recovery, but did not change in response to MOD (Fig. 3E), whereas cortisol levels were not altered by either protocol (Fig. 3F). Like cortisol, glucagon did not change during exercise, although a decline was observed after 60 min of recovery from IHE, resulting in a significant difference from MOD at this time (P = 0.027; Fig. 3G). Despite this difference in glucagon at 60 min of recovery, no difference in the ratio of glucagon to insulin was observed (Fig. 3H).


Figure 3
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  		Fig. 3. Effect of 30 min (represented by box) of MOD ({circ}) or IHE (bullet) on lactate (A), free fatty acids (B), epinephrine (C), norepinephrine (D), growth hormone (E), cortisol (F), glucagon (G), and the glucagon-to-insulin ratio (H). Results are expressed as means ± SE. a Statistically significant difference (P < 0.05) between MOD and IHE; b statistically significant difference (P < 0.05) from preexercise.

 

   DISCUSSION
TOP
 ABSTRACT
 EXPERIMENTAL PROCEDURES
 RESULTS
 DISCUSSION
GRANTS
 REFERENCES
 
This study compared the effect of IHE and MOD on the rate of glucose production and utilization during and after exercise in individuals with type 1 diabetes. It was found that IHE stimulated a more rapid and greater magnitude of increase in Ra compared with MOD. Similarly, Rd increased sooner during IHE, but by the end of exercise the total increase was comparable to MOD. During early recovery from exercise, Rd rapidly declined following IHE, whereas it remained elevated after MOD. Throughout the second hour of recovery, Ra and Rd returned to baseline following MOD but remained slightly elevated after IHE. Associated with the changes early in recovery, the GIR required to maintain euglycemia was significantly lower at this time following IHE.

The more rapid increase in Ra and Rd in response to IHE was consistent with the higher workload associated with this exercise protocol, as indicated by the greater amount of total work performed and elevation in heart rate and oxygen consumption. Since the only difference between the two exercise protocols was accounted for by the added 4-s maximal efforts involved in IHE, it is likely that these short, intense bouts were responsible for the early differences in Ra and Rd. Although the response of Ra and Rd to an isolated short bout of high-intensity exercise has not previously been investigated, it is well established that both Ra and Rd increase with exercise intensity as a result of a greater reliance on carbohydrate oxidation (37). It is also well established that, during more sustained high-intensity exercise (10–15 min at >80% VO2 max), the increase in Ra is disproportionately greater than the increase in Rd (30, 34). Although maximal efforts of only 4 s in duration are unlikely to stimulate an equivalent response, it is likely that the greater rise in Ra during IHE compared with MOD can be attributed to the repeated bouts of maximal exercise.

The mechanism by which the repeated bouts of high-intensity exercise involved in IHE stimulated a different response of Ra and Rd to exercise is likely related to the exercise-mediated changes in counterregulatory hormone levels. First, the greater early rise in Ra during IHE is likely attributed to the larger rise in norepinephrine during this protocol, since the catecholamines have been previously implicated as potent stimulators of hepatic glucose output during exercise (17), although other studies do not support this suggestion (7). On the other hand, the earlier rise in Rd during IHE might be explained by the higher intensity of exercise. High-intensity exercise typically stimulates a greater release of Ca2+ from the sarcoplasmic reticulum and activation of AMPK (5), both factors that mediate skeletal muscle contraction-stimulation of glucose transport (42). Despite this earlier rise in Rd, the total increase by the end of both exercise protocols was comparable. This may be the result of a greater reliance on muscle glycogen breakdown and, hence, increased glycolytic flux during IHE, which has been implicated as a factor that attenuates glucose Rd via glucose 6-phosphate-mediated inhibition of glucose utilization (39). It is also possible that the greater rise in norepinephrine toward the end of IHE may have attenuated the increase in glucose uptake during this type of exercise (20), as may lactate (24). Growth hormone is also elevated at this time, and although some studies have demonstrated an acute effect on glucose utilization (25, 26), most consider the effects of growth hormone on glucose turnover to take several hours to become evident (9). Furthermore, it is unlikely that insulin, glucagon, cortisol, or FFAs contributed to the differences observed in Ra and Rd during exercise, since the peripheral circulating levels of these variables were equivalent during both protocols. However, this does not preclude the possibility that different levels of these glucoregulatory factors, particularly glucagon, were present in the portal vein (38).

The exercise-induced changes in counterregulatory hormone levels might also assist in explaining, in part, the different pattern of response of Rd at the cessation of exercise. The rapid decline in Rd following IHE may be attributed to the above-mentioned higher levels of norepinephrine at this time via attenuated glucose uptake (20). Regardless, the rapid decline in Rd after IHE was surprising given that the repeated maximal sprint bouts would be expected to deplete muscle glycogen to a greater extent (14) and thus stimulate a higher rate of glucose uptake for glycogen resynthesis during recovery (29). Perhaps the high levels of norepinephrine, growth hormone, and lactate during early recovery were sufficient to counter any stimulatory effect of low glycogen levels on glucose uptake. Consistent with this interpretation, it is possible that, during the second hour of recovery, when the levels of norepinephrine, lactate, and growth hormone had returned to baseline, the raised Rd after IHE was a manifestation of increased glucose requirements for glycogen resynthesis.

The different pattern of response of Ra and Rd to IHE and MOD was relatively consistent with the changes in GIR required to maintain euglycemia. Although visual inspection of the results suggests that the increase in GIR during exercise peaked earlier and began to decline toward the end of IHE, while continuing to progressively increase during MOD, these differences were not statistically significant. On the other hand, during early recovery from IHE, the significantly lower GIR compared with MOD was consistent with the rapid decline in Rd after IHE. Finally, the increase in GIR during the second hour of recovery from IHE might be explained partly by the rise in Rd at that time. Of note, there was no significance difference in the area under the curve for GIR during exercise or recovery (results not shown).

The above-mentioned changes in Ra, Rd, and GIR in response to MOD and IHE explain only in part the previous observation that blood glucose levels decline less during and for the first hour after IHE compared with MOD (15). On the basis of this earlier study, a lower GIR was expected during IHE compared with MOD. However, as previously mentioned, no statistical difference was observed in the GIR during exercise. On the other hand, the lower GIR during early recovery from IHE is consistent with the findings of the previous study (15). Conversely, after 2 h of recovery from IHE (which was not previously investigated), the continued elevation of GIR suggests that the decline in blood glucose levels might not be less at this time after IHE if carbohydrates are not administered in the meantime.

The lack of complete consistency between the findings of the present study and the previous observation that blood glucose levels decline less with IHE compared with MOD is likely explained by differences in experimental design and the physiological conditions of study participants. First, the participants in the present study were fasted overnight, but in a postprandial state previously (15). Lower preexercise hepatic glycogen levels resulting from fasting in the present study may have impaired the exercise-induced rise in hepatic glucose production (40). Second, the circulating levels of insulin in the present study were marginally higher, which may have further attenuated the exercise-induced increase in glucose production while also enhancing glucose uptake (3). Another factor to consider is the infusion of exogenous glucose, which has been shown to attenuate glucose production and increase uptake during exercise (23). Finally, since blood glucose levels were kept stable in the present study, but allowed to decline in the real-life study (15), this might account for some of the differences in results, since the actual change in glucose level itself may be important in stimulating glucoregulatory responses (33). Thus it is advisable that future studies be conducted without glucose clamping to further elucidate the response of glucose production and utilization to these two types of exercise.

In summary, this study shows that the high-intensity bouts associated with IHE stimulate a more rapid and greater increment in endogenous glucose production during exercise than MOD alone. During early recovery from exercise, glucose utilization declines rapidly following IHE, whereas it remains elevated after MOD despite the performance of more total work. Consistent with these findings, a lower GIR required to maintain euglycemia was observed immediately following IHE compared with MOD. These events assist in explaining, in part, the previous observation that the decline in blood glucose is less with IHE compared with MOD in individuals with type 1 diabetes despite the performance of a greater amount of total work.


   GRANTS
TOP
 ABSTRACT
 EXPERIMENTAL PROCEDURES
 RESULTS
 DISCUSSION
 GRANTS
REFERENCES
 
We acknowledge the financial support of a National Health and Medical Research Council and Juvenile Diabetes Research Foundation Program Grant. Mass spectrometric analyses were carried out at the Bioanalytical Mass Spectrometry Facility, University of New South Wales (UNSW), and were supported in part by grants from the Australian Government Systemic Infrastructure Initiative and Major National Research Facilities Program (UNSW node of the Australian Proteome Analysis Facility).


   ACKNOWLEDGMENTS
 
We acknowledge the technical assistance of Leanne Youngs.


   FOOTNOTES
 

Address for reprint requests and other correspondence: K. J. Guelfi, School of Human Movement and Exercise Science, Univ. of Western Australia, 35 Stirling Highway, Crawley, Western Australia, 6009 (e-mail: kym.guelfi{at}uwa.edu.au)

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.


   REFERENCES
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 ABSTRACT
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 RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 

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