The Journal of Clinical Endocrinology & Metabolism Vol. 85, No. 8 2860-2864
Copyright © 2000 by The Endocrine Society
Impact of Time Interval from the Last Meal on Glucose Response to Exercise in Subjects with Type 2 Diabetes1
Paul Poirier2,
Angelo Tremblay,
Claude Catellier,
Gilles Tancrède,
Caroline Garneau and
André Nadeau
Québec Heart Institute at Laval Hospital (C.G., P.P.),
Diabetes Research Unit, Centre Hospitalier Universitaire de
Québec, Pavillon CHUL (P.P., C.C., G.T., A.N.), Physical Activity
Sciences Laboratory (A.T.), and Laval University, Sainte Foy,
Québec, Canada G1V 4G5
Address all correspondence and requests for reprints to: Paul Poirier, M.D., F.R.C.P.C., Québec Heart Institute, Laval Hospital, 2725 Chemin Sainte Foy, Sainte Foy, Québec, Canada G1V 4G5. E-mail:
paul.poirier{at}crhl.ulaval.ca
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Abstract
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We evaluate the influence of the time interval from the last meal on
the blood glucose response to exercise in men with type 2 diabetes.
Nineteen men with type 2 diabetes participated in an exercise training
program carried out at 60% of maximal oxygen uptake
(VO2peak) for 1 h, 3 times a week. Capillary whole
blood glucose was measured immediately before and after each exercise
session, and the time interval from the last meal (breakfast, lunch, or
dinner) was recorded. Seven time intervals were considered (fasted
overnight and 0–1, 1–2, 2–3, 3–4, 4–5, and 5–8 h postmeal). A
total of 1045 exercise sessions were analyzed. There was no change in
blood glucose levels when individuals were in the fasted state
(mean ± SE, 8.1 ± 0.2 vs.
8.1 ± 0.1 mmol/L; before vs. after, respectively).
However, blood glucose decreased by 28 ± 1% at 0–1 h, by
33 ± 1% at 1–2 h, by 35 ± 1% at 2–3 h, by 38 ±
2% at 3–4 h, by 43 ± 2% at 4–5 h, and by 23 ± 3% at
5–8 h (all P < 0.001). These results demonstrate
that 1 h of ergocycle exercise has no clinical impact on blood
glucose when performed in the fasted state in men with type 2 diabetes,
whereas a significant decrease in blood glucose should be expected when
the same exercise is performed postprandially.
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Introduction
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AEROBIC EXERCISE training has long been
considered an important part of the treatment of subjects with type 2
diabetes (1). Indeed, exercise may improve cardiovascular fitness and
assist in decreasing blood glucose levels (2). Nevertheless, little
information is available regarding the glucose level changes that occur
in subjects with type 2 diabetes after an acute bout of exercise in
relation to the time interval from the last meal.
Exercise-induced hypoglycemia in subjects with type 2 diabetes treated
with sulfonylureas is a practical concern. Health care professionals
are reluctant to instruct subjects with type 2 diabetes to exercise in
the fasted state, even though hypoglycemia during exercise tends to be
less of a problem in this population than in subjects with type 1
diabetes (2). In contrast to the belief of many practitioners (3, 4, 5, 6, 7, 8),
several studies in subjects with type 2 diabetes have shown that acute
exercise has only a modest impact on blood glucose when it is performed
in the fasted state (3, 4, 5, 9, 10, 11). Moreover, there is only one
published study that has investigated the effect of exercise on serial
glucose levels depending on the time interval from the last meal (12).
In that particular study, subjects with type 2 diabetes were treated
with diet only, and the observations made may not reflect what happens
in subjects with a more severe diabetic state requiring oral
hypoglycemic agents for their proper management. The present study was
thus undertaken to examine the impact of a 1-h exercise bout on the
blood glucose status of subjects with type 2 diabetes treated with diet
and oral hypoglycemic agents. More specifically, the influence on blood
glucose of different time intervals between the last meal and the
exercise session was evaluated in a cohort of subjects with type 2
diabetes involved in an aerobic physical training program (13).
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Subjects and Methods
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Subjects
Subjects with type 2 diabetes were enrolled in a training
program protocol that investigated the effect of physical training on
lipid profile (13). For safety purposes and to motivate the
participants, whole blood glucose levels were measured immediately
before and after each exercise session. Nineteen men with type 2
diabetes gave written consent to participate in the protocol, which was
approved by the ethics committee of Laval University. They had no
clinical evidence of diabetic complications or renal, hepatic, or
thyroid diseases. A normal treadmill exercise test (supervised by a
cardiologist) was a prerequisite for participation in the study. None
of the subjects was being treated with insulin. Except for one subject
treated with diet only, all other subjects (n = 18) were treated
with diet plus oral hypoglycemic agents (glyburide and/or
metformin). Specifically, nine subjects were treated with
glyburide alone, two were treated with metformin alone,
and seven were using a combination of both agents. None was involved in
a regular exercise program for the 6 months before entering the study.
All participants were instructed not to change their usual dietary
habits during the training period. Fasting blood was drawn from all
subjects before the exercise program for the measurement of glycated
hemoglobin (14).
Measurement of total body fat
Percent body fat was calculated from body density measured by
hydrostatic weighing using the equation of Siri (15). Fat mass was
obtained by multiplying percent body fat by body weight.
Exercise protocol
Exercise was performed three times a week, and all
sessions were under the direct supervision of an exercise physiologist.
Each session consisted of exercising on a vertical ergometer (Monark,
Stockholm, Sweden) at a workload corresponding to 60% of maximal
oxygen uptake (VO2peak). The intensity level was
prescribed and monitored on the basis of heart rate. The appropriate
heart rate was determined using the results of the
VO2peak test. Exercise duration was fixed at 30
and 45 min/session during weeks 1 and 2, respectively. From week 3, all
subjects exercised for 60 min/session. The data reported here include
values for all of these 60-min exercise sessions. The measurement of
maximal oxygen uptake was repeated after 3 months of training, and the
exercise session target heart rate was adjusted accordingly for the
following 3 months. Whole blood glucose was measured by each
participant under supervision of the exercise physiologist, immediately
before and within 5 min after the end of each exercise session with a
glucometer (One Touch, Lifescan, Inc., Burnaby, BC, Canada). The
same glucometer was used throughout the study duration, and proper
calibration procedures were followed according to the manufacturer.
Exercise sessions were performed between 0600–0900 h or later during
the day (between 1600–2000 h). The time interval between the last meal
(breakfast, lunch, or dinner) and the exercise session was recorded by
the exercise physiologist. Subjects who exercised in the fasted state
did not take their oral hypoglycemic agents before the exercise
session. Subjects attended different training sessions.
Statistical analysis
The data are presented as the mean ± SE unless
otherwise specified. One-way ANOVA was used to compare time interval
differences. When normality and/or equal variance testing conditions
were not met, the Kruskal-Wallis rank-sum test and/or Dunn’s test for
multiple comparisons were used, respectively. Pre- and postexercise
glucose level comparisons were performed using Student’s paired
t test. P 
0.05 was considered
statistically significant.
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Results
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The characteristics of the 19 subjects before the training program
are shown in Table 1
. The known duration
of their diabetes ranged from 3 months to 20 yr. As shown by the
glycated hemoglobin level, diabetes was not well controlled in many
subjects at the beginning of the study. All subjects were sedentary,
with a baseline VO2peak of 31.5 ± 5.7
mL/kg·min.
The results reflect the pooled data from the participants
throughout the program. Whole blood glucose levels were recorded from
1045 1-h exercise sessions, and 7 time intervals between the exercise
session and the last meal were considered (fasted overnight and 0–1,
1–2, 2–3, 3–4, 4–5, and 5–8 h postmeal). Table 2 depicts the number of subjects, the
number of exercise sessions, the percentage of target heart rate
attained, and the percentage of blood glucose decrease from baseline
for each time interval. The percentage of target heart rate attained
was slightly lower when exercise was performed in the fasted state or
during the first hour following a meal (Table 2). Interestingly, the
decrease in blood glucose from baseline was most pronounced when
exercise was performed 3–5 h after the last meal (Table 2).
Figure 1 shows the glucose levels before
and after aerobic exercise at different time intervals from the last
meal. There was no change in whole blood glucose levels (before
vs. after) after exercise when participants were in the
fasted state (mean ± SE, 8.1 ± 0.2
vs. 8.1 ± 0.1 mmol/L, respectively). However, when
participants had consumed a meal before exercise, blood glucose levels
decreased significantly (P < 0.001). Of particular
interest is that even if preexercise blood glucose levels were
comparable in the fasted state and 5–8 h postprandially, blood glucose
levels decreased significantly only in subjects who were in the
postprandial state (8.2 ± 0.4 decreasing to 6.0 ± 0.2
mmol/L; P < 0.001). Moreover, the blood glucose
response to exercise in relation to the previous meal did not differ
between the first 3 months and the last 3 months of the exercise
training protocol (data not shown). No subject suffered from clinical
hypoglycemia during the exercise session. However, few exercise
sessions (n = 14) ended with a blood glucose level of 3.3 mmol/L
or less (range, 2.8–3.3 mmol/L), and all of them were carried out in
the postprandial state.
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Figure 1. Glucose levels before and after 1 h of
aerobic exercise at 60% of VO2peak based on the time
interval from the last meal (fasted overnight, n = 80 sessions;
0–1 h, n = 351 sessions; 1–2 h, n = 254 sessions; 2–3 h,
n = 88 sessions; 3–4 h, n = 126 sessions; 4–5 h, n =
102 sessions; 5–8 h, n = 44 sessions). *, P
< 0.001, before vs. after.
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To lessen the impact of the number of exercise sessions performed per
individual in each time interval, the averaged blood glucose changes
for each subject for each time interval were compared. Results remained
essentially the same. There was no significant change in whole blood
glucose levels (before vs. after) after exercise in the
fasted state (8.6 ± 0.6 vs. 8.1 ± 0.5 mmol/L;
P = 0.536). However, subjects showed a significant
decrease in blood glucose levels after exercise at 0–1 h (10.7 ±
0.6 vs. 7.5 ± 0.5 mmol/L), 1–2 h (10.8 ± 0.7
vs. 7.0 ± 0.5 mmol/L), 2–3 h (10.0 ± 1.1
vs. 6.2 ± 0.7 mmol/L), 3–4 h (10.1 ± 0.8
vs. 6.2 ± 0.4 mmol/L), 4–5 h (9.2 ± 0.8
vs. 5.5 ± 0.4 mmol/L; all P < 0.001),
and 5–8 h (9.0 ± 1.0 vs. 6.1 ± 0.5 mmol/L;
P = 0.003). Furthermore, we analyzed our data on the
basis of treatment for diabetes. We separated our group into three
subgroups; 1) glyburide alone, 2) glyburide
plus metformin, and 3) metformin plus diet alone. The results held
firm. There was no significant decrease in capillary blood glucose when
subjects exercised while fasting in each group: glyburide
alone, 7.6 ± 0.2 vs. 7.6 ± 0.2 mmol/L;
glyburide plus metformin, 7.8 ± 0.2 vs.
7.9 ± 0.2 mmol/L; and metformin plus diet, 9.2 ± 0.3
vs. 9.0 ± 0.3 mmol/L.
To provide further evidence, we isolated data from four subjects who
performed at least nine exercise sessions in the fasted state and at
0–1 h postprandially. These individuals performed 76% of the total of
all exercise sessions carried out in the fasted state and 49% of all
exercise sessions carried out 0–1 h after a meal. Again, blood glucose
levels did not decrease significantly when exercise was performed in
the fasted state (7.7 ± 0.2 vs. 7.8 ± 0.1
mmol/L, before vs. after, respectively) in contrast to a
significant decrease seen at 0–1 h (10.1 ± 0.2 vs.
7.6 ± 0.1 mmol/L; P < 0.001).
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Discussion
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This study demonstrates that 1 h of exercise performed at
about 60% VO2peak did not decrease whole blood
glucose levels when performed in the fasted state by men with type 2
diabetes treated with diet and oral hypoglycemic agents. However, a
decrease of 20–40% from baseline was experienced when exercise was
performed in the postprandial state.
These results agree with previous investigations that have shown no
major effect of exercise on blood glucose when exercise is performed in
the fasted state by subjects with type 2 diabetes (3, 4, 5, 10), in
contrast to the frequent belief of many health care professionals.
Apart from the nutritional status, numerous factors, such as the
intensity and duration of the exercise session, the type of treatment,
and metabolic control, may also influence the blood glucose response
after exercise in subjects with type 2 diabetes.
Indeed, exercise intensity and duration interact with regard to
the decline in plasma glucose concentrations in subjects with type 2
diabetes. It has been shown that changes in plasma glucose levels are
similar after 70 min of exercise at 50% VO2peak
compared to 50 min at 70% of VO2peak (7).
Furthermore, it has been clearly demonstrated that the longer the
exercise session, the greater the decline in blood glucose levels when
exercise is performed at the same intensity in subjects with type 2
diabetes (11). Looking at the type of treatment and blood glucose
control, the glycemic response to exercise tends to be greater in
patients treated with diet only than in those treated with oral
hypoglycemic agents (9, 11). Moreover, the decline from baseline
glucose is greater in subjects who start exercise with higher fasting
blood glucose (7, 8, 11). In this regard, it is of interest to note
that in the present study subjects who exercised 5–8 h after a meal
decreased their blood glucose much more than those who exercised in the
fasted state, even if they had similar preexercise blood glucose
levels. Although blood glucose decreases with increasing time interval
from the last meal, exercise still potentiates the blood glucose
decline seen normally after a meal in all time periods considered. The
percentage of target heart rate achieved was approximately 5% lower in
subjects who exercised in the fasted state than in those who had
consumed a meal 5–8 h before exercise. However, the percentage of
target heart rate was also about 5% lower in subjects who exercised at
0–1 h after the ingested meal, but those individuals nevertheless
experienced a significant decrease in blood glucose levels. Considering
results from previous investigations (3, 4, 5, 9, 10, 11), it is unlikely that
the 5% lower percentage of target heart rate could account for the
difference in results between subjects who exercised in the fasted
state and postprandially.
There is a potential increased risk of hypoglycemia with exercise in
patients with type 2 diabetes receiving sulfonylurea therapy. The risk
is generally perceived by clinicians to be greater when exercise is
performed in the fasted state (4, 5, 10). However, in daily life,
physical exercise is usually performed in the postprandial rather than
the fasted state. Because hypoglycemia can precipitate myocardial
ischemia (16), knowledge about the expected decline in blood glucose
after exercise is important. Thus, it is primordial to know the impact
of the nutritional status on blood glucose response after exercise. It
has been reported that with concomitant oral agent administration,
exercise performed 1 h in the postprandial state (breakfast)
decreased blood glucose levels by 10–15%, and only a few subjects
experienced hypoglycemia in a cohort of subjects with well controlled
type 2 diabetes (17). On the other hand, no significant decrease in
blood glucose was observed in other studies in subjects with well
controlled type 2 diabetes when exercise was performed in the fasted
state when the subjects had not taken their usual oral hypoglycemic
agents for at least 36 h before the study (4, 5). In the present
study subjects had not taken their medication before exercising in the
fasted state, as usually advised in such situation. Moreover, due to
the long duration of action of glyburide (16–24 h), this
medication was probably still acting in some subjects (18). Blood
glucose levels were examined in those (n = 5) who had taken
glyburide at dinner the day before exercise and in those
(n = 5) who did not. There was no difference between those two
subgroups of subjects in the blood glucose change with exercise.
Moreover, the treatment for diabetes does not seem to influence the
blood glucose response to exercise while fasting. It is important to
note that subjects from previous studies and the present one were
mildly hyperglycemic (8–12 mmol/L) before the exercise session in the
fasted state and that no hypoglycemia occurred in these individuals as
in the present study (3, 4, 5, 6, 7, 8, 9, 10, 11, 12). Of interest, in the present study the few
exercise sessions that ended with the lowest blood glucose levels were
encountered when subjects performed exercise in the fed state.
Regular exercise is considered one of the cornerstones in the
management of patients with type 2 diabetes. Indeed, exercise is
recommended as a nonpharmacological means to improve lipid profile (13)
and insulin sensitivity (2, 19). However, long-term compliance to an
exercise program is low (20, 21), and motivation incentive needs to be
developed. Lowering of blood glucose may be used as part of the
motivation, and knowledge about the degree of lowering that can be
expected postprandially with exercise will help both in motivating
subjects to exercise regularly and in prescribing a safe exercise
program.
Limitations
Numerous variables may have influenced the response to
exercise. Unfortunately, the study design does not allow us to assess
the macronutrient and calorie compositions of each meal. Although there
is important variability in the blood glucose responses related to a
particular meal in subjects with type 2 diabetes, this study was
intended to be representative of an out-patient setting. The present
study does not allow uncovering the mechanism by which blood glucose
levels decreased when exercise is performed after a meal in contrast to
the fasted state, when blood glucose levels did not change
significantly. Nevertheless, one possible explanation could be that the
hepatic glucose production is diminished by the meal-induced insulin
response, thereby creating an imbalance between glucose production and
glucose utilization in the fed state and causing a decline in blood
glucose levels (12, 22, 23). Conversely, stable insulin levels in the
fasted state may allow the increased glucose utilization to be
adequately matched by a parallel increase in glucose production, which
results in a blunted blood glucose decline. Obviously, further research
is needed to determine the underlying mechanism behind our observations
to optimize the impact of exercise on glucose control in subjects with
type 2 diabetes. Of interest, however, is that these observations were
obtained in an out-patient clinical settings, such as these patients
and health care professionals use to interact daily. Obviously, further
research with standardized meal, similar drug regimens, and formal
ascertainment of time interval from meal to exercise and/or drug intake
is needed to determine the underlying mechanism behind our observations
to optimize the impact of exercise on glucose control in subjects with
type 2 diabetes.
In summary, the results of this study conducted in men with type
2 diabetes have shown that 1 h of ergocycle does not cause a
decrease in whole blood glucose when performed in the fasted state
before taking the oral agents, whereas it does so when the same
exercise stimulus is applied after a meal. Thus, contrary to a frequent
belief, the risk of a hypoglycemic event may be greater when subjects
with type 2 diabetes performed exercise after a meal than in the fasted
state, although no serious events occurred with the 1045 exercise
sessions reported in the present study.
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Acknowledgments
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We appreciated the assistance of H. Bessette with the
measurement of maximal oxygen uptake. We also thank Dr. R. Larouche
(deceased) for exercise testing. We express our gratitude to Dr.
William T. Donahoo for interesting discussion during the preparation of
this manuscript.
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Footnotes
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1 This work was supported by Health and Welfare Canada. 
2 Recipient of a Medical Research Council of Canada
studentship.
Received November 15, 1999.
Revised April 21, 2000.
Accepted May 14, 2000.
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Top
Abstract
Introduction
