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The Effect of Postprandial Exercise on Meal-

related Glucose Intolerance in Insulin-
dependent Diabetic Individuals

Article in Diabetes Care · July 1982

DOI: 10.2337/diacare.5.4.364 · Source: PubMed

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 T he Effect of Postprandial Exercise on
Meal-related Glucose Intolerance in
Insulin-dependent Diabetic Individuals
D. CARON, P. POUSSIER, E. B. MARLISS, AND B. ZINMAN
Although exercise is a central therapeutic modality in insulin-dependent diabetic patients, its prescrip-
tion and expected effects have remained far less precise than the concurrent modalities of insulin and
diet. To quantify the potential benefit of exercise on meal glycemic excursions, eight insulin-dependent
diabetic subjects were studied on two separate days during breakfast and lunch, with and without 45 min
of moderate exercise, starting 30 min after breakfast. All other variables were kept constant, including
their usual insulin doses, which were given subcutaneously in the abdomen. Fasting glycemias were
brought to comparable levels by overnight insulin infusion (rest day: 110 ± 9 mg/dl; exercise day:
105 ± 9 mg/dl). Postprandial exercise reduced peak glycemia for breakfast (270 ± 22 versus
203 ± 22 mg/dl) and lunch (270 ± 16 versus 170 ± 20 mg/dl, P < 0.05) for the group as a whole on rest
day and exercise day, respectively. Three types of individual responses were seen. Five subjects showed
an improved glycemic excursion with exercise during both breakfast and lunch. In two subjects only the
lunch response was significantly improved. One subject showed no effect of exercise. The failure to
demonstrate a lowering of glycemia with breakfast appears to be related to the persistent use of fat-
derived fuels in these subjects. This is suggested by a lower respiratory quotient (RQ), and elevated free
fatty acid and 3-hydroxybutyrate concentrations. Plasma "free" insulin and glucagon concentrations
could not account for these observations. Thus, the majority of subjects showed improved glucoregula-
tion related to exercise performed postprandially. If adequately insulinized, conventionally treated dia-
betic individuals can benefit from strategically timed exercise, DIABETES CARE 5.- 364-369, JULY-AUGUST 1982.

E
xercise has been considered an important compo- the time of exercise. Hepatic glucose production is inhibited
nent of the treatment of diabetes since the early in the face of accelerated muscle glucose uptake and glyce-
demonstrations of its glucose-lowering effect.1'2 As mia decreases.5 In contrast, with insulin deficiency, exercise
a therapeutic modality, however, it has been un- results in an increase in glycemia and accelerated ketone
derused and imprecisely applied due to lack of precise data as body production.3 Interestingly, when insulin is administered
to predicated metabolic effects. Although recent studies with by a constant basal intravenous infusion sufficient to main-
insulin-dependent diabetic individuals have shown variable tain normoglycemia at the onset of exercise, a normal glu-
responses, often depending on the particular experimental coregulatory response to exercise is observed.5 Thus, it is
design,3"7 they have provided important insight into the dif- evident that the metabolic and hormonal milieus at the
ferences in the metabolic responses in diabetic subjects as onset of exercise are important variables in determining the
compared with normal controls. It is well known that a de- response.
crease in glycemia during exercise with the potential of de- The present study was undertaken to quantify the acute ef-
veloping symptomatic hypoglycemia can occur in insulin- fects of exercise, in a situation designed to simulate "real-
treated diabetic persons particularly if the depot injection life" as closely as possible, on abnormal glucoregulation in
site is an exercising extremity.5'8 This appears to be related insulin-dependent diabetic persons. Postprandial glycemic
in part to hyperinsulinemia as a consequence of accelerated excursions were examined in subjects who received their
insulin absorption in response to muscle contraction or any usual insulin therapy, with and without a 45-min period of
other circumstances resulting in peripheral insulin excess at moderate exercise after breakfast.

364 DIABETES CARE, VOL. 5 NO. 4, JULY-AUGUST 1982

 POSTPRANDIAL EXERCISE ON MEAL GLUCOSE INTOLERANCE/D. CARON AND ASSOCIATES

METHODS blood sampling on the morning of the experiment, after an

overnight fast of 12-14 h.
Subjects. Eight insulin-dependent diabetic individuals were Each subject was studied twice, with and without exercise
studied in the Clinical Investigation Unit and Respiratory in random order, with an interval of 2 days during which
Research Laboratory of the Toronto General Hospital. The multiple injections of crystalline zinc insulin were contin-
five men and three women were nonobese, actively em- ued. On the study days, the subjects were given their usual
ployed, and had diabetes from 8 to 24 yr duration with a morning insulin dose (Table 1) subcutaneously in the abdo-
mean of 16.2 ± 1 . 6 yr. They were all on a weight-maintain- men, 30 min before breakfast; the intravenous insulin infu-
ing diet based on the Canadian Diabetes Association (CDA) sion was stopped 15 min before breakfast.
pattern. The diabetic subjects were on no medication other The subjects ate breakfast and lunch corresponding to the
than insulin, except two patients (nos. 7 and 8), who had amounts prescribed for outpatients based on the CDA pat-
been on replacement L-thyroxine for more than 10 yr. There tern. The mean caloric content of the meals for the group
was no clinical or laboratory evidence of significant diabetic was 447 ± 67 kcal (47% carbohydrate, 35% fat, 18% pro-
complications, and all subjects had normal exercise EKGs. tein) for breakfast and 550 ± 80 kcal (39% carbohydrate,
Maximum work capacity was estimated during steady-state 35% fat, 26% protein) for lunch. Breakfast was at time 0 and
exercise on a bicycle ergometer at two different work loads, lunch at 240 min. On the "rest" day, subjects remained sed-
measuring oxygen uptake and heart rate.9 Anthropomorphic entary and were monitored until 210 min after lunch. On
and physical fitness data are given in Table 1. Informed con- the "exercise" day, the insulin dose, the site of injection,
sent was obtained in compliance with the requirements of and the meals were identical to those of the rest day; how-
the Human Experimentation Committee of the University of ever, 30 min after the start of breakfast, exercise was begun
Toronto. and continued for 45 min on a bicycle ergometer (Siemens-
Protocol. On the day of admission to the Clinical Investi- Elema model 380, Stockholm, Sweden) at a work load calcu-
gation Unit, intermediate-acting insulin was discontinued lated to result in pulmonary oxygen uptake of approximately
and glycemic control was maintained by multiple subcutane- 50% of the previously estimated maximum value.
ous injections of crystalline zinc insulin for 48 h. Before For respiratory measurements, the subjects breathed
each study, euglycemia was achieved and maintained over- through a two-way, low-resistance, low-dead-space (9 cc)
night by intravenous infusion of insulin in physiologic saline pulmonary function laboratory breathing valve (W. E. Col-
with a volumetric infusion pump (Imed Canada Inc., Missis- lins, Boston, Massachusetts) into a system fitted with a fan to
sauga, Ontario, Canada). ensure complete mixing of the expired gases. Respiratory gas
A 20-gauge catheter with an obturator (B.D. Intravenous concentrations were measured with rapid response CO 2 (LB-
Catheter and Obturator, Becton-Dickinson, Rutherford, 2)- and O 2 (OM-ll)-analyzers (Beckman Instruments Inc.,
New Jersey) was introduced into an antecubital vein for Palo Alto, California). After thorough flushing of the dead

TABLE 1
Anthropomorphic and clinical data

Age % Ideal Predicted max. Work load Duration of Insulin

Patient (yr) Sex Wt (kg) Ht (cm) weight* VO 2 (ml/kg/min) (W) IDDM (yr) type Dose (U)

K.Y. 20 F 60 169 +1 25.0 40 8 Lente 26

Regular 8
j.P. 22 M 73 180 +5 45.2 120 19 Lente 50
R.K. 27 M 61 175 -6 32.7 70 24 NPH 32
C.W. 21 M 77 170 + 10 48.9 140 19 Lente 20
Regular 10
D.S. 21 M 65 165 +6 34.7 80 15 Lente 28
Regular 14
R.J. 37 M 66.5 175 0 32.0 70 16 Lente 32
Regular 10
C.K. 20 F 53 158 +4 49.0 100 13 Lente 20
Regular 10
A.M. 26 F 79 172 + 15 28.9 70 16 NPH 28
Regular 8

* Based on the Metropolitan Life Insurance Company Tables, 1959.

DIABETES CARE, VOL. 5 NO. 4, JULY-AUGUST 1982 365

 POSTPRANDIAL EXERCISE ON MEAL GLUCOSE INTOLERANCE/D. CARON AND ASSOCIATES

space of the breathing valve, tubing, and Tissot gas meter, fast glycemia peaked at 270 ± 22 mg/dl at 95 min, and de-
two 2-min collections of expired gas were made at rest. VO 2 ,creased to 203 ± 22 mg/dl at 240 min. With lunch, peak
VCO 2 , minute ventilation, EKG, and heart rate were moni- glycemia (257 ± 16 mg/dl) was reached at 360 min, remain-
tored in the resting state just before exercise, at 5, 15, 30,ing at a plateau until the end of the sampling period. On the
and 45 min of exercise, and during recovery at 15 and 30 min exercise day, a similar response was seen for 30 min after
as detailed previously. breakfast. However, with exercise, the rise in glycemia was
attenuated and remained constant during exercise at
nalytic methods. Plasma glucose was determined using 190 ± 33 mg/dl. Thereafter, glycemia decreased to
a glucose analyzer (Beckman Instruments, Inc.), 163 ± 30 mg/dl just before lunch. After the second meal, all
and blood 3-hydroxybutyrate was assayed in values from 300 min onward were significantly lower with
perchloric acid supematants by an enzymic mi- exercise as compared with the rest day.
crofluorometric method.10 Plasma free fatty acids (FFA) were The three types of individual glycemic responses that con-
determined by the radiochemical microtechnique of Ho. 11 tributed to the mean results shown in Figure 1 are demon-
The assay for "free" insulin was performed on polyethylene Glycemia During Meals ! Exercise
glycol supematants of plasma after incubation at 37°C for
12 LUNCH
2 h, using insulin antibody supplied by Dr. Peter Wright, I
purified human insulin standard, and 125I-labeled pork insu-
lin (Novo Research Laboratory, Copenhagen, Denmark).
Plasma glucagon was measured by a single-antibody, char-
coal-precipitation radioimmunoassay with glucagon anti-
serum 30K obtained from Dr. Roger Unger. Student's un-
paired t test was used to compare the meal responses with and
without exercise.

RESULTS

Respiratory data. Pulmonary oxygen uptake (VO2) and car-

bon dioxide output (VCO2) increased five- to sixfold with
exercise. Resting heart rate was 85 ± 4 beats/min and in-
creased to a peak 151 ± 5 beats/min with exercise.
Glycemia. The glycemic response to breakfast and lunch
with and without exercise is shown in Figure 1. On both
days, fasting glycemias were comparable (rest versus exercise:
110 ± 9 versus 105 ± 9 mg/dl). On the rest day, the break-

Glycemia During Meals * Exercise

c
BKF LUNCH SUBJECT R K
350
I I
300 I EXERCISE I

* — " * ^ - o — - « > Eurciia

250

a 200

a
150

100

100
60 120 180 240 300 360 420
50
r
0 60 120 16 240 300 360 420 480 540

Minutes FIG. 2A-C. Glycemic responses during breakfast {BKF) and lunch at
FIG. I. Glycemic responses during breakfast (BKF) and lunch at restrest ( • — • ) , and with 45 min of bicycle ergometer exercise beginning 30
( • - — • ) , and with 45 min of moderate bicycle ergometer exercise begin-
min after BKF (O—O). The responses of three individual subjects are
ning 30 min after BKF (O—O). Mean and SEM are shown. shown.

366 DIABETES CARE, VOL. 5 NO. 4, JULY-AUGUST 1982

 POSTPRANDIAL EXERCISE ON MEAL GLUCOSE INTOLERANCE/D. CARON AND ASSOCIATES

Free Insulin During Meals ± Exercise insulin profiles throughout the day. The pattern was one of a
3.5
slow progressive increase of levels with a delayed and slightly
higher peak on the exercise day (3.3 ± 0.3 ng/ml at 270 min
3.0
with exercise versus 2.9 ± 0.3 ng/ml at 115 min without ex-
ercise, P = NS). Glucagon concentrations were similar at
rest in the two protocols (time 0 min glucagon rest versus ex-
2.5
ercise: 183 ± 41 versus 166 ± 129 pg/ml). The only signifi-
cant change with exercise was a small postexercise peak at 95
2.0
and 115 min (342 ± 24 versus 270 ± 12 pg/ml, P < 0.05).
Fuel utilization during exercise. Free insulin, fat-derived sub-
C 15
strates, and respiratory quotient (RQ) in the subjects who
showed an improved exercise-related glycemic response to
1.0
breakfast (group 1) are compared with those of subjects who
did not (group 2) in Table 2. Measurements taken immedi-
0.5
ately before exercise (pre-exercise, 30 min after the start of
breakfast) and at the end of the exercise period (postexer-
0.0
60 120 180 240 300 360 420 cise) are shown. Free insulin concentrations were similar.
Minutes However, 3-hydroxybutyrate and free fatty acid concentra-
FIG. 3. Free insulin (F/RJ) concentrations during breakfast (BKF) and tions were elevated both pre- and postexercise in group 2.
lunch at rest ( • — • ) , and with 45 min of bicyck ergometer exercise The RQ was also lower, indicating proportionally greater
beginning 30 min after BKF ( O — O ) (1 ng/ml = 25 fiU/ml). Mean lipid oxidation than in group 1.
and SEM are shown.

strated in Figure 2. A marked improvement in the abnormal DISCUSSION

glycemic excursion to breakfast and lunch occurred in 5 of 8

E
subjects, as illustrated by subject D.S. (Figure 2A). In 2 sub- xercise has long been accepted as an important
jects, there was no change in breakfast glycemia, but a signif- component in improving diabetic control. How-
icant improvement in the lunch response was exemplified by ever, its use in the treatment of diabetes has been
subject C.W. (Figure 2B). One subject (R.K.) showed no imprecise. This has been related in part to a poor
beneficial effect of exercise on either meal (Figure 2C). understanding of the exercise responses seen in diabetic indi-
viduals and to a concern regarding exercise-induced hypogly-
"Free" insulin and glucagon. The results of the plasma
cemia.
"free" insulin concentrations are shown in Figure 3. The
fasting values were similar (rest versus exercise: 2.5 ± 0.3 Most previous studies of the diabetic patient's responses to
versus 2.3 ± 0.2 ng/ml, 1 ng/ml = 25 /aU/ml) as were the exercise were performed in the overnight-fasted state and the
variable responses seen often reflected varying degrees of in-
sulin excess or deficiency. The aim of the present study was
TABLE 2 to determine if exercise could be used specifically in the post-
Insulin, fat-derived substrates, and RQ* during exercise
prandial state to improve the hyperglycemic responses to
3-Hydroxy- meals characteristic of diabetes. The variables of meal size
Free insulin butyrate and composition, intensity, type, timing, and duration of ex-
(ng/ml) (MM) FFA {fxM) RQ ercise, insulin dosage, and injection site, and starting glyce-
mia were controlled, with the patient being studied on two
Group 1
occasions that differed only by the inclusion of postprandial
(N = 4)
110 ± 35 550 ~ 110 0.84 ± 0.03
exercise.
Pre-exercise 2.44 ± 0.15
Postexercise 2.18 ± 0.30 88 ± 25 530 :: 130 0.86 ± 0.02 Not surprisingly, the glycemic responses of the group as a
Group 2 whole to breakfast were improved by exercise performed 30
(N = 3 ) min after the start of that meal. This response likely resulted
Pre-exercise 2.26 ± 0.40 400 ± 170 850 ± 60 0.70 ± O.Olt from at least two independent factors: (1) a reduction in
Postexercise 2.30 ± 0.65 315 ± lOOt 930 ± 135 0.76 ± 0.04 splanchnic blood flow occurs with the onset of exercise, and
the absorption of nutrients from the gastrointestinal tract
Group 1: Diabetic subjects with exercise-related decrease in breakfast may be slowed and (2) the absorbed glucose is preferentially
glycemia. used by the exercising muscle as a metabolic fuel. The latter
Group 2: Diabetic subjects without exercise-related change in breakfast
mechanism is supported by data on regional metabolism dur-
glycemia.
Measurements were made immediately before exercise (pre-exercise, which
ing mild exercise after ingestion of a glucose load13 and stud-
corresponds to 30 min after the start of breakfast) and at the end of the ies of postprandial exercise in normal human beings and in-
exercise period (postexercise). sulin-infused diabetic individuals.14 An RQ consistent with
* Respiratory exchange ratio. oxidation principally of carbohydrate (Table 2, group 1) be-
t P < 0.05, group 2 versus group 1. fore and after exercise supports this hypothesis. However, in

DIABETES CARE, VOL. 5 NO. 4, JULY-AUGUST 1982 367

 POSTPRANDIAL EXERCISE ON MEAL GLUCOSE INTOLERANCE/D. CARON AND ASSOCIATES

three subjects breakfast glycemic excursions were entirely ciated. The excellent secretarial assistance of Maria Rotkop
unaffected by exercise. Although starting glycemias were is gratefully acknowledged.
similar, this subgroup was characterized by higher 3-hydroxy- These studies were supported by a grant (MA 5767) from
butyrate and free fatty acid concentrations and a lower RQ the Medical Research Council of Canada.
both before and after exercise. These metabolic differences
were consistent with the continued use of fat substrates as an This paper was presented in part in abstract form at the Amer-
energy source despite meal ingestion and marked hyperglyce- ican Federation for Clinical Research: Eastern Section Meeting,
mia, and suggested deficient insulin action. "Free" insulin October 26, 1981 (Clin. Res. 29: 681A).
levels were not significantly different, however, and did not From the Department of Medicine, Toronto General Hospital,
correlate to the type of glycemic responses observed. Assum- University of Toronto, Toronto, Ontario, Canada.
ing the methodology for free insulin determination truly re- Address reprint requests to B. Zinman, Toronto General Hospi-
flects the biologically effective insulin as indicated by previ- tal, 101 College Street, Toronto, Ontario M5G 1L7, Canada.
ous studies reporting physiologically meaningful values,15'16
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368 DIABETES CARE, VOL. 5 NO. 4, JULY-AUGUST 1982

 POSTPRANDIAL EXERCISE ON MEAL GLUCOSE INTOLERANCE/D. CARON AND ASSOCIATES

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DIABETES CARE. VOL. 5 NO. 4, JULY-AUGUST 1982 369