(Chest. 2000;117:47-51.)
© 2000
American College of Chest Physicians
Beneficial Effect of Short-term Endurance Training on Glucose Metabolism During Rehabilitation After Coronary Bypass Surgery*
Piotr Dylewicz, MD, PhD;
Slawomira Bienkowska, MD;
Lucja Szczesniak, PhD;
Tadeusz Rychlewski, MD, PhD;
Izabela Przywarska, MD;
Malgorzata Wilk, MSc and
Andrzej Jastrzebski, PhD
*
From the University School of Physical Education, Institute of Rehabilitation, Department of Cardiac Rehabilitation, Rehabilitation Hospital, Poznan, Poland.
Correspondence to: Piotr Dylewicz, MD, PhD, Rehabilitation Hospital, Department of Cardiac Rehabilitation, ul. Nad Jeziorem 2, 60–480 Poznan, Poland; e-mail: cardreh{at}soho-online.com
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Abstract
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Aims: Our study was aimed at determining whether
beneficial modification of carbohydrate metabolism can be obtained
after a short-term training program and whether it is associated with
an increase in binding and degradation of 125I-insulin by
erythrocyte receptors that suggests a decrease in insulin
resistance.
Methods: The study was conducted in a
group of 20 patients aged 56 ± 1.9 years (mean ± SEM), within 1
to 6 months after coronary bypass surgery. All patients completed 15
training sessions based on 30 min of cycling with a constant load.
Before and after a 3-week training program, glucose, insulin, and
C-peptide blood levels, as well as binding and degradation of
125I-insulin by erythrocyte receptors, were
determined.
Results: A statistically significant
decrease was found in the blood glucose level, from 111.2 ± 4.2 to
97.8 ± 3.5 mg/dL (p < 0.01); this decrease was not accompanied by
significant insulin concentration changes. There was also a significant
increase in insulin binding, from 0.535 ± 0.059 to 0.668 ± 0.042
pg 125I/1011 RBCs (p < 0.01), and
degradation from 7.64 ± 0.54 to 9.49 ± 0.58 pg
125I/1011 RBCs (p < 0.05).
Conclusion: The results indicated that even short-term
endurance training in patients rehabilitated after coronary bypass
surgery induced favorable modification of glucose metabolism,
presumably caused by a decrease in insulin resistance.
Key Words: coronary bypass surgery • endurance training • insulin resistance
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Introduction
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Coronary
artery bypass surgery does not eliminate the risk factors for coronary
heart disease, which promote further progression of atherosclerosis in
coronary arteries and may also contribute to coronary artery bypass graft atheroclerosis and graft
occlusions.1
2
3
Insulin resistance and hyperinsulinemia
are considered independent risk factors for cardiovascular
disease.4
5
In 1989, Foster6
described
insulin resistance as a "secret killer." Barnard et
al7
studied the influence of physical training and diet on
the insulin resistance phenomenon in patients with an impaired glucose
tolerance test and provided evidence that physical training reduces
insulin resistance. Investigations conducted in patients after
myocardial infarction showed that physical training, continued for 1
year, decreased insulin blood level.8
However, a
short-term (3-week) endurance training program conducted in patients
after myocardial infarction decreased insulin blood level only in
subjects with hyperinsulinemia.9
In patients rehabilitated
after coronary bypass surgery, no significant changes in insulin blood
level have been found in response to physical training, while the
glucose blood level has been seen to substantially decrease compared
with patients who have not exercised.10
The authors of the
latter publication did not investigate insulin resistance indicators
and suggested only that the observed decrease in glucose blood level
after exercise training is related to a decrease in insulin
resistance.10
The results in patients who have undergone
coronary bypass surgery need to be verified by more detailed research
with respect to the above-mentioned metabolic risk factors. This is
necessary because in recent years, in general only patients with severe
pathology and multivessel disease are referred for coronary bypass
surgery. Therefore, we have undertaken studies to establish whether
improvement of glucose metabolism in patients rehabilitated after
coronary bypass surgery depends on lowering of insulin resistance in
response to physical training. Also, we were interested in determining
whether such an effect can already be detected after a short-term
rehabilitation course, and if it is associated with improvement in
physical performance and in blood lipid profile.
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Materials and Methods
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The study was conducted in a group of 20 men between 33 and 68
years of age, with a body mass index (BMI) of 26.49 ± 0.81
kg/m2, 1 to 6 months after coronary bypass
surgery (mean, 3.8 months). This investigation was performed after
receiving the approval of patients and the Regional Ethics Board of the
Committee for Science and Research.
Patients with an ejection fraction of < 35% who did not reach at
least 75 W in a preselection symptom-limited exercise test (test 1)
were eligible to participate in the study. Patients who demonstrated
signs of angina pectoris or severe arrhythmia or had diabetes mellitus
were excluded from our study. Forty percent of studied individuals were
hypertensive, with BP well controlled by drugs.
After the preliminary examination, the second symptom-limited
exercise test (test 2) was carried out on the following day to
establish the individual load applied in the training program. It was
accompanied by the analysis of oxygen consumption and
CO2 output using a CardiO2
analyzer with a CPX-D computer system (Medical Graphics Corp; St. Paul,
MN). The exercise test started with a load of 25 W and increased by 25
W every 3 min. The ventilatory threshold was determined by the
computerized V-slope method described by Beaver et al,11
with software supplied by Medical Graphics. Before the test and 3 min
after its completion, capillary blood from the pulp of the finger and
venous blood from the basilic vein were taken.
The following parameters in the capillary blood samples were measured:
acid-base balance on the AVL 995 Hb analyzer (AVL Scientific Corp;
Roswell, GA); lactate level by the Boehringer Mannheim test (Boehringer
Mannheim Corp; Indianapolis, IN); and glucose level by the Cormay
Company test (Cormay Company; Lublin, Poland). The samples of
venous blood plasma were analyzed for insulin level by radioimmunoassay
with double antibodies using radioimmunoassay insulin sets, and for
C-peptide level using the Biodat-Serono test (Biodat-Serono;
Serono, Italy). The erythrocytes were isolated from heparinized
blood, and 125I-insulin binding and degradation
by erythrocyte receptors were determined according to the method
described by Gambhir and Nerurkar.12
After the initial
investigation, the whole group of patients underwent training for 3
weeks. Each patient received identical dietary instructions according
to European Atherosclerosis Society recommendations.13
The first stage of the training sessions was continuous endurance
training on a bicycle ergometer. The training started not earlier than
2 h after a meal and was preceded by a medical examination every
day. The training load was applied for 3 weeks, 5 times a week (15
training units altogether). The duration of each training unit was 30
min and included 5 min of warming up (riding a bicycle without the
load); 20 min of riding with the load; and 5 min of active rest (riding
a bicycle without the load). Training was performed with the load at
10% below the load obtained at the ventilatory threshold during the
cardiopulmonary exercise test carried out after the preliminary
examination. BP and pulse were systematically recorded during each
training unit. Three to 5 days after the beginning of the training
program, lactic acid levels were measured following the termination of
the training session in order to evaluate whether the training exertion
was performed under aerobic conditions. In no case did the lactic acid
levels determined exceed the threshold values. In addition, patients
participated in overall conditioning exercises for 30 min daily, along
with 30 to 60 min of walking.
After 3 weeks, the analyzed parameters were reexamined according to the
protocol. The third exercise test (test 3), involving gas exchange
analysis, was stopped at the same workload as in the second test. One
day before discharge from the hospital, the fourth consecutive exercise
test (test 4), of the symptom-limited type, was performed. This was
introduced to assess the differences in the amount of work before and
after the training course.
During the study period, patients continued the same drug treatment
they used before admission to the hospital.
Statistical Analysis
Results are expressed as mean value ± SEM. To compare the
data within the same group before and after the training program, the
Wilcoxon test was used. To compare the data between the groups, the
Mann-Whitney test was applied. A value of p < 0.05 was considered
significant.
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Results
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Physiologic parameters measured at rest and at the end of the
cardiopulmonary exercise test (test 2 and test 3), before and after a
3-week rehabilitation course, are listed in Table 1
. No major variations were recorded in either the resting or exercise
heart rate before and after the training program. However, a
significant decrease was found in the resting and exercise systolic BP,
from 143.20 ± 4.97 mm Hg to 129.10 ± 5.63 mm Hg (p < 0.05) and
from 193.60 ± 6.07 mm Hg to 168.20 ± 4.64 mm Hg (p < 0.01),
respectively. Similarly, resting diastolic BP was noticeably reduced,
from 94.50 ± 2.65 mm Hg to 85.50 ± 3.40 mm Hg (p < 0.05). The
marked decrease in rate-pressure product (from 24,344 ± 1,361 to
19,910 ± 1,449; p < 0.001) was accompanied by a significant
reduction in the lactic acid blood level in the final exercise test
(from 3.34 ± 0.26 mmol/L to 2.93 ± 0.17 mmol/L; p < 0.05).
Mean BMI was 26.49 ± 0.81 kg/m2 before the
training program and 26.69 ± 0.84 kg/m2 at the
final examination.
During the 3-week physical training period (15 training sessions), a
significant improvement was observed in physical performance, as
expressed by a substantial increase in the amount of work achieved in
the symptom-limited exercise test. The average amount of work was
23.7 ± 1.8 kJ in the preliminary examination (test 2) and
33.0 ± 2.4 kJ (p < 0.001) at the end of training program (test 4;
Table 2
). Also the maximal physical performance and duration of the exercise
symptom-limited test after the rehabilitation course increased
significantly, from 91.2 ± 4.3 W to 112.0 ± 5.2 W and from
7.3 ± 0.3 min to 9.1 ± 0.4 min, respectively (Table 2)
. Table 3 demonstrates the average fasting plasma concentrations of carbohydrate
metabolism parameters and indicators of insulin resistance measured at
rest. Short-term physical training markedly decreased the glucose
concentration, from 111.2 ± 4.2 mg/dL to 97.8 ± 3.5 mg/dL
(p < 0.01). Generally, the insulin serum level did not change
substantially, and the simultaneously measured C-peptide blood level
increased significantly from 2.38 ± 0.25 ng/mL to 3.1 ± 0.45
ng/mL (p < 0.05). Both the binding and degradation of
125I-insulin by erythrocyte receptors in examined
patients increased during exercise training, from 0.535 ± 0.059 to
0.668 ± 0.042 pg125I/1011 RBCs for binding
(p < 0.01), and from 7.64 ± 0.54 to 9.49 ± 0.58 pg
125I/1011 RBCs for
degradation (p < 0.05).
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Table 3.. Parameters of Carbohydrate Metabolism and Insulin
Resistance Before and After the 3-Week Rehabilitation Course*
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The changes in carbohydrate parameter values were accompanied by a
statistically significant decrease in the total cholesterol blood
level, from 213.5 ± 12.6 mg/dL to 199.7 ± 10.3 mg/dL
(p < 0.05; Table 4
). There were no substantial correlations between the changes in
parameters of carbohydrate metabolism and lipid metabolism during the
rehabilitation course. The change in high-density lipoprotein
cholesterol blood level was correlated with a change in the amount of
tolerated exercise load (r = 0.62; p < 0.01). Otherwise, no other
correlations between improvement of metabolic parameters and increase
in physical performance were recorded.
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Discussion
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Our study revealed that even a short-term period of physical
training in patients rehabilitated after coronary bypass surgery,
besides resulting in an improvement in exercise tolerance, leads to
beneficial modification of glucose metabolism and the advantageous
alteration of lipid metabolism parameters. This corresponds with the
study undertaken by Ágren and coworkers,10
who also
observed a beneficial metabolic modification, as expressed by a
decrease in blood glucose level detected only in patients engaged in
the exercise program. They did not observe the same tendency in a group
of untrained patients. Our data confirm the hypothesis of Ágren
et al10
that favorable carbohydrate metabolic modification
is probably associated not with a decrease in insulin secretion, but
rather, mainly with an increase in receptor affinity to insulin. Such a
suggestion can be put forward on the grounds of the observation that
after training, the C-peptide level increases commensurate with the
increase in insulin secretion. If the insulin level has not been
significantly elevated in spite of the increase in insulin secretion,
it could mean that insulin binding to receptors may have been
increased; this may be an indicator of reduction of insulin resistance.
This suggestion has been confirmed by the present study, which showed
an increase in binding and degradation of
125I-insulin by erythrocyte receptors. We used
the model of Gambhir et al, a relatively simple clinical test that is
easier to use in the assessment of rehabilitation than the glucose
clamp applied in the evaluation of insulin
sensitivity.12
14
It is important to note that RBCs are
not a typical site for the action of insulin because the main target
areas are skeletal muscles and adipose tissue. The insulin-binding
characteristics of insulin receptors on erythrocytes are comparable to
those on myocytes and adipocytes, and it has been corroborated that
defects in insulin binding correlate with insulin
sensitivity.15
16
Because the training started an average of 3.8 months after surgery in
our study, it can be implied that favorable results in exercise
capacity and also in glucose and lipid metabolism were not dependent on
convalescence time but, rather, that they were mainly the effect of
physical training. Such a conclusion can be drawn from the work of
Dubach et al,17
who reported that a considerable
spontaneous increase in exercise capacity generally occurs up to 2
months after coronary bypass surgery.
It is interesting that the alteration of lipid profile relates better
to the improvement in physical performance than changes in glucose
metabolism. Previous studies showed that the increase in insulin
resistance was related to a rise in triglyceride blood
level.18
We consider that, in the case of our patients, physical training alone,
and the diet only to a small extent, had an influence on this
modification. This is suggested by the lack of change in BMI, which
was, in fact, slightly higher at the final investigation. The
information obtained from the questionnaire survey also indicates that
during the rehabilitation course, the patients only partly adhered to
dietary recommendations.
The observation time of 3 weeks is short, and the beneficial effects of
physical training may be transient.19
20
The studies
carried out by Björntorp et al8
in patients
undergoing rehabilitation for 1 year after myocardial infarction
indicated that a reduction in the insulin blood level is permanent. It
would appear that this favorable effect of a decrease in resistance to
insulin-mediated glucose disposal in patients after coronary bypass
surgery can be also sustained throughout the continuation of physical
exercise.
It is suggested that insulin resistance can be the underlying cause of
other risk factors of coronary heart disease, such as arterial
hypertension, obesity, type II diabetes (ie,
non-insulin-dependent diabetes mellitus), hypercholesterolemia, and
hypertriglyceridemia.5
21
This suggestion has not been
accepted indisputably, and confirmation of these associations is needed
from further studies.16
However, we cannot rule out the
possibility that insulin resistance may intensify the development of
atherosclerosis in coronary arteries, leading to ischemic heart
disease, even if it does not influence the functioning of grafts. Thus,
it seems that the issue of beneficial modification of insulin
resistance is one of the arguments suggesting that endurance training
on a bicycle ergometer may be useful for the secondary prevention of
coronary heart disease in patients who have undergone coronary bypass
surgery, especially in patients with substantial pathology of the
carbohydrate and lipid metabolism.
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Footnotes
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Abbreviations: BMI = body mass
index
Received for publication November 24, 1998.
Accepted for publication August 18, 1999.
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Abstract
Introduction
