ClinicalScience (1 970) 38’1-9.
T H E EFFECTS O F ISOCALORIC E X C H A N G E O F
DIETARY STARCH A N D SUCROSE O N GLUCOSE
TOLERANCE, PLASMA I N S U L I N A N D S E R U M LIPIDS
IN M A N
M. G. D U N N I G A N , T . F Y F E , * M. T. M c K I D D I E t
AND
S. M. CROSBIE
Atheroma Research Unit $, Western Infirmary, Glasgow
(Received 3 May 1969)
S UMMA R Y
1. The effects of isocalorically exchanging dietary starch and sucrose on glucose
tolerance, plasma insulin and serum lipids were examined in nine middle-aged
subjects. A ‘sucrose’ period in which 70% of dietary carbohydrate was supplied as
sucrose was alternated with a ‘sucrose free’ period in which dietary carbohydrate
was supplied mainly as starch. Each period lasted 4 weeks; eleven balances were
completed.
2. Changes in body weight during the balances were small and statistically insignificant.
3. Fasting blood sugar levels were significantly elevated during the ‘sucrose’
period. During 50 g glucose tolerance tests, blood sugar levels were slightly higher
during the ‘sucrose’ period but this difference was not statistically significant.
4. Plasma insulin levels were similar during the dietary periods, both in the fasting
state and after 50 g of glucose.
5. Mean levels of serum cholesterol, serum triglyceride and plasma NEFA showed
no significant differences between the two dietary periods.
6. It is concluded that glucose tolerance, plasma insulin and serum lipids are not
significantly altered by the substitution of sucrose for starch at levels of sucrose
intake comparable to those in the Western diet.
It has been convincingly shown that dietary carbohydrate influences serum lipids in man,
particularly serum triglyceride (Ahrens et al., 1961 ; Antonis & Bersohn, 1961). Sucrose has
attracted particular interest because of its postulated relationship with ischaemic heart disease
(Yudkin, 1964; Yudkin & Morland, 1967) and because of possible differences between the
effects of sucrose and complex carbohydrates on serum lipids (Macdonald & Braithwaite,
* Present address:Victoria Infirmary, Glasgow.
t Present address: Royal Infirmary, Glasgow.
Now Blood Pressure Research Unit.
Correspondence:Dr M. G. Dunnigan, Western Infirmary, Glasgow, W.l.
1
2
M . G. Dunnigan et al.
1964; Groen et al., 1966; Antar & Ohlson, 1965; Kuo & Bassett, 1965; Kaufman et al., 1967).
Less attention has been paid to the comparative effects of simple and complex carbohydrates
on carbohydrate metabolism. Only two studies (Macdonald & Braithwaite, 1964; Cohen et al.,
1966) appear to have examined the comparative effects of sucrose and starch on glucose
tolerance in man.
The present study examines the effects of isocalorically exchanging dietary starch and
sucrose on glucose tolerance, plasma insulin and serum lipids in nine middle-aged subjects.
Sucrose intakes were comparable to those of the normal Western diet.
MATERIALS A N D METHODS
Six men and three women, aged from 37 to 62 years, participated in the study, which was
carried out in the metabolic ward of the Atheroma Research Unit. Three separate balances
were carried out on one subject (S.M.) at intervals of 12 and 7 months to assess the reproducibility of the results in a single individual; eleven balances were carried out in all. Eight patients
suffered from chronic neurological disease (parkinsonism, M.A., H.L., S.M. ; disseminated
sclerosis, J.C., J.F., G.F., cerebro-vascular disease, S.W.). Their disabilities were stable,
continued stay in hospital being determined mainly on social grounds. The remaining subject,
E.D., suffered from coronary artery disease. All subjects could eat normally. All had normal
carbohydrate tolerance as judged by a 50 g glucose tolerance test carried out on normal ward
diet. Three subjects (G.F., M.A., E.D.) had moderately elevated cholesterol levels and one
(E.D.) moderate hyperglyceridaemia. The three patients with parkinsonism (M.A., H.L.,
S.M.) had been stabilized on benzhexol for many years and this was maintained during the
balance. There is no evidence that this drug affects carbohydrate or lipid metabolism. No other
drugs were used during the study.
Each balance lasted for 10 weeks. Following 2 weeks on ward diet, subjects were placed on a
fixed caloric intake. Estimated energy expenditure was based on each subject’s calculated basal
metabolic rate together with daily ward activities. The accuracy of the estimate was checked
by regular weighing.
Protein, fat and carbohydrate formed 15%, 40% and 45% of the caloric intake. Polyunsaturated fats comprised 5% of the total fat intake. During one period of 4 weeks (the ‘sucrose’
period) 70% of dietary carbohydrate was supplied as sucrose, 22% as starch and 8% as other
mono- and disaccharides (glucose, fructose and lactose). Daily sucrose intakes ranged from
1 18 to 210 g with a mean of 169 g. These are of the same order as the reported sucrose intakes
of United Kingdom and Canadian subjects (Marr & Heady, 1964; Papp, Padilla & Johnson,
1965). The ‘sucrose’ period was alternated with a ‘sucrose free’ period of 4 weeks duration, in
which 85% of dietary carbohydrate was given as starch and 15% as mono- and disaccharides
(other than sucrose). Starch was supplied as wheat or potato starch with a small quantity of
maize starch. In five balances (E.D., H.L., M.A., J.C. and S.M.(i)) the ‘sucrose’period was first,
in six it was second. There was no interval between the ‘starch’ and ‘sucrose’ periods. The
frequency of taking sucrose was identical to that of starch, food being supplied as three meals
and three snacks daily. Saccharin was used in tea or coffee while on starch feeding and the
starch equivalent of sugar in tea given as unsweetened biscuits.
During the balances serum cholesterol, serum triglyceride and blood sugar were estimated
thrice weekly after an overnight fast in all subjects, except that during the first balance (S.M.(i))
Isocaloric exchange of starch and sucrose
3
blood sugar estimations were carried out only twice weekly. In seven balances fasting plasma
insulin levels were also measured thrice weekly and 50 g glucose tolerance tests were carried out
weekly, blood sugar and plasma insulin being estimated +,1, 1+ and 2 hr after glucose. In the
remaining four balances plasma non-esterified fatty acids (NEFA) were estimated thrice weekly
in the fasting state. This plan was adhered to as closely as possible; the actual numbers of
observations made are indicated in Tables 1-5.
A Technicon AutoAnalyzer was used to estimate serum cholesterol (Method N24P). A
control serum of known concentration was analysed with every twelve tests. A correction
factor obtained from the actual and expected standard serum reading was applied to the results
from each batch of tests to eliminate daily or long-term instrumental variation. Serum triglycerides were measured in duplicate by the method of Van Handel & Zilversmit (1957) using a
triolein standard. Plasma NEFA was measured in duplicate by a modification of the Dole
method (Dole & Meinertz, 1960) using a palmitic acid standard. Blood sugar was measured
on a Technicon AutoAnalyzer (Method N2b). As a check on instrumental variation, a standard
serum was analysed daily, commercial control sera of known value were analysed weekly, and
regional control sera were analysed monthly. Plasma insulin was measured in duplicate by an
immunoassay technique (Hales & Randle, 1963) in the Department of Medicine, Glasgow
Royal Infirmary. A detailed account of experience of this method in the latter department
with reference to sensitivity, precision and specificity has been previously given (Buchanan &
McKiddie, 1966).
RESULTS
Weight
Changes in weight during each balance are shown in Table 1. Overall changes were small
indicating that the actual energy expenditure of the group was close to the estimated figure.
One subject (R.W.) showed a marked weight gain during the ‘sucrose free’ period which was
largely lost during the ‘sucrose’period.
Carbohydrate tolerance
Levels of fasting blood sugar were significantly higher (Pc 0.001) during the ‘sucrose’ period
of the eleven balances considered together (Table 2, Fig. 1). The mean difference, though small,
is rendered highly significant by the large number of observations on which it is based (n =
246). Considering the balances separately, fasting blood sugars were significantly elevated in
five out of eleven cases. In only two balances were fasting blood sugar levels lower during the
‘sucrose’ period and these differences were not statistically significant.
In the seven balances in which glucose tolerance tests were carried out at weekly intervals,
levels of fasting blood sugar were significantly higher (P<0-02) during the ‘sucrose’ period.
Blood sugar levels during the glucose tolerance tests were slightly higher during the ‘sucrose’
period but the differences were not statistically significant (Table 3). In contrast to the findings
for fasting blood sugar, fasting levels of plasma insulin for the ‘sucrose’ and ‘sucrose free’
periods were almost identical. Levels of plasma insulin after glucose showed small differences
which were not significant (Table 3). Comparison of the ‘area’ under each blood sugar and
plasma insulin curve (Jarrett & Graver, 1968) also failed to show statistically significant
differences between the two dietary periods. It may be noted that for the seven balances in
M . G . Dunnigan et al.
4
TABLE
1. Subjects’ age, sex and initial weight, with weight changes during
the ‘sucrose’ and ‘sucrose free’ periods of each balance
Change in weight (kg)
Subject
sex and age
S.M.(i)
S.M.(ii)
S.M.(iii)
S.W.
E.D.
H.L.
M.A.
J.C.
J.F.
G.F.
R.W.
Mean
M49
M50
MSO
M61
F60
F60
F62
M49
M49
M43
M37
Initial weight
(kg)
65.3
63.3
60.2
41.5
60.2
67.7
57.8
63.7
56.8
82.3
75.7
63.1
‘Sucrose’
period
‘Sucrose free’
period
- 0.9
- 1.5
- 0.9
- 1.5
- 1.1
- 1.2
- 0.9
1.6
0
- 0.4
-0.4
3.4
0.3
- 0.2
- 0.4
0.3
0.4
-0.5
- 3.5
0.7
+
+
+
+ 0.7
+ 1.3
+ 5.3
+
+
+
- 0.7
TABLE
2. Mean levels of fasting blood sugar during the ‘sucrose’ and ‘sucrose
free’ periods of each balance
Mean fasting blood sugar k SEM
Subject
‘Sucrose’ period ‘Sucrose free’ period
(mg/100 ml)
(mg/100 ml)
S.M.(i)
S.M.(ii)
S.M.( iii)
n
P
15
< 0.05
NS
R.W.
74.3 f 1.5
71.2f 3.0
83.4 k 1.2
74.6f 1.1
72.7+ 2.5
66.3+ 1.2
67.6k 3.8
75.0f 2.5
72.7 k 2.0
1 5 8 f 1.9
78.4k 1.6
61.9 f 1.9
15.7 f2.2
77.2+ 1.6
65.4 3.6
66.2 f 1.9
64.8 f 2.2
68.3 & 1.4
74.3f 1.7
69.0 f 1.2
69.7f 1.6
70.0 k 1.9
24
24
21
21
22
23
24
24
24
24
Mean
74.0 k 0.8
70.0 _+ 0 6
246
S.W.
E.D.
H.L.
M.A.
J.C.
J.F.
G.F.
<0.01
< 0.05
NS
NS
NS
NS
NS
< 0.05
<0.01
< 0.001
Isocaloric exchange of starch and sucrose
5
sucrose free’
period
90.
85
-
80
2
E
s
\
-; 75
b
s
p
70
-
.-P
eIn
65
60
..
..
55
1
401
FIG.1. Individual values for fasting blood sugar during the ‘sucrose’ and ‘sucrose free’ periods of
eleven balances. Mean blood sugars? SD are indicated.
TABLE
3. Glucose tolerance and plasma insulin during the ‘sucrose’ and ‘sucrose free’ periods of seven balances
Mean plasma insulin_+SEM
Mean blood sugar _+ SEM
Time after
50 g glucose
Fasting
4 hr
Ihr
It hr
2 hr
‘Sucrose’
period
(mg/100 rnl)
‘Sucrose free’
period
(mg/100ml)
75+ 1
113_+3
113+4
91 + 4
73+3
‘Sucrose’
period
(b units/ml)
‘Sucrose free’
period
(p unitslml)
n
P
<002
26+ 1
NS
NS
NS
NS
130_+11
137+15
95+ 13
25+1
121-122
133+15
164
55
54
94+8
55
56?7
56
NS
NS
NS
NS
NS
n
P
72+1
108+3
167
56
109+4
89?3
71+3
54
55
56
54? 7
M . G . Dunnigan et al.
which glucose tolerance tests were performed weekly, estimations of fasting blood sugar and
plasma insulin exceed the number after glucose (Table 3); this is due to the former estimations
being performed thrice weekly.
Serum lipids
Serum cholesterol and triglyceride levels for the group as a whole showed no significant
changes between the ‘sucrose’ and ‘sucrose free’ periods of the balance (Table 4). Plasma
NEFA also showed no significant change in the four subjects in whom it was measured
(Table 5).
TABLE
4. Mean levels of serum cholesterol and serum triglyceride during the ‘sucrose’ and ‘sucrose free’ periods
of each balance
Mean serum cholesterol f SEM
Subject
Mean serum triglyceride f SEM
‘Sucrose’
period
(mg/100 ml)
‘Sucrose free’
period
(mg/100 ml)
n
P
‘Sucrose’
period
(mg/100 ml)
‘Sucrose free’
period
(mg/100 ml)
n
P
S.M.(i)
S.M.(ii)
S.M.(iii)
S.W.
E.D.
H.L.
M.A.
J.C.
J.F.
G.F.
R.W.
270-16
236f 3
220 -14
181 f 4
263 2 7
275? 12
296f8
17923
222 -19
295 -13
135f1
267 -1 10
245 f4
221 f 3
18023
247 f5
278 f 3
261 f5
155-18
217f2
310f 6
142f2
26
24
22
25
24
24
24
22
24
24
23
Mean
234f 5
23125
262
NS
NS
NS
NS
NS
NS
< 0.01
< 0.01
NS
NS
< 0.01
NS
70f 2
5024
69-13
73f4
188f8
109-17
76f2
111f4
96f 5
100f4
78f3
93f3
67f4
62-13
64-13
69f2
187+8
113f4
73f3
1062 10
82f4
108f5
78f4
92f3
25
24
24
24
24
24
24
23
22
24
23
261
NS
< 0.05
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
TABLE5. Mean levels of plasma non-esterified fatty acids (NEFA)
during the ‘sucrose’ and ‘sucrose free’ periods of four balances
Mean plasma NEFA f SEM
Subject
‘Sucrose’ period
S.M.(i)
S.W.
E.D.
H.L.
Mean
(ml/l)
‘Sucrose free’
period (pEq/l)
n
P
611f35
355 30
475 f 28
387 2 26
447f21
417f27
568 f 39
382 f 34
450 f 25
450f 18
23
21
22
22
88
NS
NS
NS
NS
NS
Isocaloric exchange of starch and sucrose
7
Serum cholesterol levels were in two subjects (M.A. and J.C.) significantly higher and in one
subject (R.W.) significantly lower during the ‘sucrose’ period. One subject (S.M.) showed
significantly lower levels of the triglyceride during the ‘sucrose’ period of his second balance
(Table 4). These changes bore no relationship to changes in weight between the two periods
of the balance (Table 1). They are not obviously attributable to differences in either the composition or caloric content of the ‘sucrose’ and ‘sucrose free’ diets. Technical factors seem
unlikely to be responsible. Watkin et al. (1954) and Wolf et al. (1962) observed variations in
serum cholesterol of the same order as found in the present study in some in-patient subjects
maintained under controlled conditions of diet and exercise; Wolf et al. (1962) attributed the
variations to emotional environmental stress. The significant changes in serum lipids noted in
the present study probably represent similar biological variations unrelated to the experimental
diet under test.
DISCUSSION
Close in-patient supervision seems essential during this type of study in order to achieve strict
control of dietary intake. Long-stay hospital patients were used for this reason (with one
exception; E.D.) since healthy subjects are normally not amenable to confinement for the
prolonged periods required. The disabilities from which our subjects suffered were stable and
did not constitute a variable in the investigation. They were metabolically normal except
for the moderately elevated lipid levels shown by three subjects. While not ideal, they appeared
suitable for an investigation of this kind.
Macdonald & Braithwaite (1964) found no alteration in glucose tolerance in three subjects
on a low fat diet in whom carbohydrate was supplied either as sucrose or as uncooked maize
starch. Cohen et al. (1966) found that in sixteen normal out-patient subjects on a low fat diet,
the isocaloric replacement of sucrose for bread starch caused significant impairment of glucose tolerance. Plasma insulin levels were not measured. In the present investigation, the small
but significant elevations of fasting blood sugar during the ‘sucrose’ period constituted the
only consistent difference between the two dietary periods. Plasma insulin levels showed no
significant change; in particular, fasting plasma insulin levels were closely similar. It may be
concluded that the isocaloric exchanges of starch and sucrose carried out in the present
study were without significant effect on the insulin secreting mechanism. However, since the
changes in fasting blood sugar were small, small concomitant changes in plasma insulin cannot be excluded, since the method for assaying the latter is less precise than that for blood
sugar. It remains possible that the significant changes in fasting blood sugar were due to an
alteration in glucose homeostasis which is independent of insulin; the possible mechanism of
such an alteration must be speculative.
Serum cholesterol and triglyceride levels do not appear to be affected by interchanging
dietary sucrose and starch at sucrose intakes within the range of the normal Western diet.
The results of the present study agree with our earlier conclusions (Dunnigan, Fyfe & Sawers,
1967) and are similar to the findings of Grande, Anderson & Keys (1965), Lees (1965) and
Antonis (1967). They are at variance with those of Macdonald & Braithwaite (1964), Groen
et al. (1966) and Antar & Ohlson (1965) who found clear-cut differences between the effects
of starch and sucrose on serum lipids. The reason for these discrepancies is not clear. Antonis
(1967) suggested that significant changes in serum lipids might be produced by small but important differences in caloric intake between the ‘starch’ and ‘sucrose’ periods of these studies.
M . G . Dunnigan et al.
The present investigation does not support this hypothesis since there was no correlation between changes in weight and in serum lipids for the two periods of the balance. None of our
subjects was as grossly hyperlipaemic as those of Kuo & Bassett (1965) and Kaufman et af.
(1967) who showed marked changes in serum lipids with isocaloric starch/sucrose substitutions.
Changes in serum lipids may occur in gross hyperlipaemia which are not evident in normolipaemic or even moderately hyperlipaemic subjects (Anderson, 1967 ;Grande, 1967).
Except for small but significant changes in fasting blood sugar, the present study suggests
that carbohydrate tolerance and serum lipids are not altered by the substitution of starch for
sucrose within the normal range of sucrose intakes. There remains a need for long-term comparative studies of starch and sucrose feeding to establish if differences in glucose tolerance
and serum lipids will arise which are not evident in the short-term experiments carried out to
date.
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