Clinical Science (1972)43,265-214.
RELATIONSHIP BETWEEN DIETARY
CARBOHYDRATES A N D FATS I N THEIR I N F L U E N C E
O N SERUM LIPID CONCENTRATIONS
I. MACDONALD
Department of Physiology, Guy’s Hospital Medical School, London
(Received 26 January 1972)
SUMMARY
1. Diets containing 45% joules as fat, 45% joules as carbohydrate and 10% joules
as calcium caseinate were given for 5 days to ten men and seven women. The fats
used were sunflower seed oil or cream, and the carbohydrates were either glucose
and fructose, glucose and raw starch or fructose and raw starch.
2. Sunflower seed oil in the diet resulted, after 5 days, in a significant fall in the
concentration of triglyceride, cholesterol and phospholipid in the serum taken from
subjects fasted for 12 h irrespective of the carbohydrate mixture of the diet.
3. Although there were changes in serum lipid concentrations in relation to the
different mixtures of carbohydrate they were much less than those seen after ingesting
sunflower seed oil.
4. Men and women differed in their response to carbohydrates, but this distinction
was not seen in response to dietary fats.
Key words : dietary fats, dietary carbohydrates, serum lipids.
Saturated fat in the diet is frequently associated with a rise in the serum cholesterol concentration whereas polyunsaturated fat in the diet may decrease a raised serum cholesterol
concentration (Keys, 1970). Also, dietary carbohydrate can raise the concentration of triglycerides in the serum of fasting subjects (Ahrens, Hirsch, Little, Farquhar & Stein, 1961).
Little work, however, has been reported on the interrelationship of fat and carbohydrate in the
diet with lipid metabolism. It has been reported that the increase in triglyceride level of fasting
serum in response to dietary sucrose can be modified by the type of fat in the diet both in
normal men (Macdonald, 1967) and hypertriglyceridaemic patients (Antar, Little, Lucas,
Buckley & Csima, 1970).
The experiments described in the present paper were done to learn to what extent the type of
dietary fat could influence the response of serum lipids in fasting subjects to various dietary
carbohydrate mixtures.
Correspondence: Professor I. Macdonald, Department of Physiology, Guy’s Hospital Medical School.
London, S.E.1.
265
I. Macdonald
MATERIALS A N D METHODS
Ten healthy male dental students aged 18-21 years volunteered to subsist on a liquid formula
diet composed of carbohydrate (45% of joules), fat (45% of joules) and calcium caseinate
protein (10% ofjoule intake). One vitamin capsule (B.P.C.)was taken by each subject on each
day during the dietary period, which lasted 5 days. There was an interval of at least 10 days
between each diet, and each subject participated in all six experimental diets.
The intake of formula diet was approx. 170 J day-' kg body weight-' and was adjusted
to keep the body weight constant.
As a difference in the triglyceride response to dietary carbohydrate has been observed
between men and pre-menopausal women (Macdonald, 1965) it was also decided to give
seven young women aged 18-21 years diets similar to those given to the men.
The fats used were sunflower seed oil or double cream (48%volume = fat). The carbohydrate
mixtures used were either: (a) 40% fructose and 60% raw corn starch, (b) 40% fructose and
60% glucose, or (c) 40% glucose and 60% raw corn starch. The carbohydrates were mixed
in this way because it is not possible to use fructose as the sole source of dietary carbohydrate,
as it may cause diarrhoea.
Samples of serum were obtained after a 12 h fast on the morning the diet started and on the
penultimate and final mornings before the subject returned to his free-choice diet. The triglyceride (Lofland, 1964), phospholipid (Krehl, Lopez & Good, 1967) and cholesterol (Block,
Jarret & Levine, 1966) estimations were semi-automated.
TABLE
1. Weight and 'declared' normal intakes of the men before the experimental period
(values calculated from McCance & Widdowson, 1960)
Subject
S.M.
A.W.
D.D.
J.W.
T.G.
M.M.
E.H.
P.M.
M.G.
J.T.
Mean
Weight
(kg)
Protein
(g)
Fat
(9)
Carbohydrate
(g)
Sucrose
(9)
84
78
13
75
18
75
72
93
73
68
77
100
90
75
80
75
105
80
90
120
85
110
120
100
95
105
155
110
120
135
135
119
235
305
280
300
190
365
365
395
375
345
316
50
25
70
85
5
25
125
150
80
95
10
25
55
30
10
10
60
71
90
Alcohol
(g)
Energy content
(cal)
(kJ)
2400
2850
2700
5
20
2600
2100
3350
3200
3300
3200
2950
10.1
12.0
11.3
10.9
8.8
14.1
13.4
13.9
13-4
12-4
27
2865
12.0
40
RESULTS
Men
The weight of each subject and average dietary intake before the experiment are seen in
Table 1.
Lipid concentration in serum during fasting. The mean values for each subject obtained
during fasting from six serum samples on the day each diet started are seen in Table 2. Due to
J.T.
T.G.
M.M.
E.H.
P.M.
M.G.
J.W.
S.M.
A.W.
D.D.
Subject
79
103
83
68
83
122
106
213
96
84
4.4
4.2
4.5
6.3
4.2
6.4
10.3
9.9
10.2
7.9
161
222
193
139
183
154
191
199
189
178
7-2
9-1
8.0
6.8
2-7
4.0
5.7
12-1
5-2
10.6
SE
Mean
SE
Mean
Cholesterol
Triglyceride
Men
10.4
13-9
14.2
9.2
12.9
12.2
14.3
15.4
18.5
15.6
SE
J.R.
R.B.
J.S.*
A.S.
D.W.
A.C.
J.T.
Subject
95
107
84
70
102
109
70
Mean
9.8
6.5
-
6.0
6.4
6.2
5.0
SE
Triglyceride
* Subject partook of three experimental diets only.
175
244
193
156
201
152
198
202
181
169
Mean
Phospholipid
201
208
168
158
229
221
198
Mean
5.4
3.2
3.1
9.7
3.4
4.5
SE
Cholesterol
Women
148
160
143
134
166
155
142
-
5.8
5.3
5.5
11.4
4.7
5.3
Mean SE
Phospholipid
70
50
51
59
6 0
61
68
Weight
(kg)
TABLE
2. Mean of six values of the pre-diet concentration (mg/lOO ml) of triglyceride, cholesterol and phospholipid in serum from fasting subjects
f
t.l
g%
3
GI
%
4
k!
$
0
.;r
?I
a
"-c-
Sunflower seed oil,
fructose, starch
Cream, fructose, starch
Sunflower seed oil,
fructose, glucose
Cream, fructose,
glucose
Sunflower seed oil,
glucose, starch
Cream,glucose,starch
Diet
-10
+13
-23*
-5
-24*
+22*
10
10
10
10
Mean
-6
-25*
+26*
2.9
5.1
-29*
-12*
$22
Mean
4.1
10.3
4.8
3.8
3.7
11.5
SE
Day 5
3.2
4.0
61
7.2
SE
Day 4
10
10
n
Trig1yceride
* P < 0.025.
-23*
-1
-2
-27*
-17*
+8*
Mean
2.0
2.3
1.2
1.9
2.0
2.3
SE
Day 4
-28*
f3
-1
-30*
-22*
+12*
Mean
1.9
2.3
1.7
2.3
2.6
2.6
SE
Day 5
Cholesterol
TABLE3. Mean percentage change in serum lipid fractions after fasting in men
-28*
-16
-5
-21*
-33*
+8*
Mean
3.0
6.5
3.4
4.1
3.7
2.3
SE
Day 4
-27*
-12
0
-30*
-39*
+12*
Mean
2.1
6.2
2.9
1.5
3.2
2.6
SE
Day 5
Phospholipid
5
269
Fats, carbohydrates and serum lipids
wide individual range of values the changes after 4 and after 5 days on each experimental diet
for each lipid component were expressed, for every subject, as a percentage rise or fall from
his mean fasting value. The mean values of each of these percentage changes in each lipid
fraction for each experiment diet are seen in Tables 3 , 4 and 5.
Triglyceride (Table 3). The triglyceride concentration in the serum taken from subjects
fasted for 12 h fell significantly after 5 days on the diet containing sunflower seed oil, whereas
on the diet containing cream, glucose and starch there was a significant rise in the fasting
triglyceride concentration after days 4 and 5.
To assess differences between diets the percentage change in the lipid fraction produced by
one diet on day 4 and on day 5 was subtracted from the corresponding value for that individual
on comparable days while on another diet. The mean of the ten values for each day, so obtained,
was tested using Student’s t test for significant difference from zero.
Fructose -Glucose
d
+ 20
s
c
s
?
Starch -Glucose
d
c
+ 12
+4
0
-4
- 12
- 20
J
s
?
c
s
c
r
FIG. 1. Mean percentage difference in serum triglyceride concentrations between diets. S, sunflower seed oil;C, cream. Shaded area, P<O.O25.
When this was done for the triglyceride concentration in serum from fasting subjects, it was
found that after ingestion of sunflower seed oil, the triglyceride concentration was higher when
fructose was in the diet than when glucose was in the diet. This effect was not seen with cream
in the diet. Also, with both dietary fats the triglyceride concentration in the serum was higher
when starch replaced glucose (Fig. 1).
Cholesterol (Table 3). As expected the cholesterol concentration decreased when sunflower
seed oil was in the diet.
By subtracting the results for each subject on one diet from the results in the same subject
on another diet it was found that on all the carbohydrate diets the cholesterol concentration
after the sunflower seed oil diet was approx. 30% lower than after the cream diet. The diets with
cream contained cholesterol (1-2 mg/ml).
I. Macdonald
270
Fructose
s
+ 16
d
c
Starch
- Glucose
s
sqc
- Glucose
dc
sqc
+ 12
+8
+4
I
0
-4
-8
FIG.2. Mean percentage differencein serum cholesterol concentrations between diets. S, sunflower
seed oil; C, cream. Shaded area, P<0.025.
Fructose - Glucose
Starch - Glucose
I
d
c4
s
d
c
s
?
c
s
c
0
-4
- 12
- 20
- 28
FIG.3. Mean percentage difference in serum phospholipid concentrations between diets. S, sunflower seed oil; C, cream. Shaded area, P<O.O25.
Sunflower seed oil,
fructose, starch
Cream,fructose,starch
Sunflower seed oil,
fructose, glucose
Cream, fructose,
glucose
S d o w e r seed oil
glucose, starch
Cream,glucose,starch
Diet
-32*
+10
-18
fl
-31*
-4
6
6
7
7
Mean
7.1
64
7.0
7.7
7.7
11.4
SE
Day 4
7
6
n
-34*
-11
0
-18*
-37*
-2
Mean
48
5.5
6.0
5.1
6.8
11.3
SE
Day 5
Triglyceride
2.4
2.2
-18*
-2
* P<0.025.
2.4
1.9
3.3
1.7
SE
i-3
-25*
0
-13*
Mean
Day 4
-22*
-2
+4
-26'
-18*
4-2
3.1
3.0
2.9
2.4
1.9
3.8
SE
Day 5
Mean
Cholesterol
TABLE
4. Mean percentage change in serum lipid fractions after fasting in women
-27*
-8
-5
-23*
-27*
-4
Mean
SE
2.6
3.9
41
5.7
2.3
6.1
Day 4
2.7
4.0
4.4
-8
-29.
-9*
5.6
2.5
6.4
SE
-27*
-30*
-14
Mean
Day 5
Phospholipid
3
2
&
9
H
2
h
9
t,
%
s8
f3
c,
u-
272
I. Macdonald
The cholesterol concentration in subjects on fructose diets was about 10% higher than the
concentration in subjects on glucose diets and this was highly significant. Similarly subjects on
starch-containing diets had serum cholesterol concentrations about 10% higher than those on
glucose-containing diets (Fig. 2).
Phospholipid (Table 3). The concentration fell significantly in subjects on all the diets
containing sunflower seed oil. Compared with the cream-containing diets, the phospholipid concentration was about 25% lower in subjects on the sunflower seed oil-containing
diets.
There was no difference in the effect of starch- and glucose-containing diets on phospholipid
concentrations, but fructose-containing diets were associated with a lower phospholipid
concentration than dietary glucose, when cream was in the diet (Fig. 3).
Women
There was no significant change in the weight of the subjects while they were on any of the
diets. The dietary intake of each subject before the experimental diets was not evaluated.
The method of expressing the change in the serum lipid fractions was the same as that used
in the data for men and the mean values of the serum lipid concentration obtained during
fasting before each experimental period are shown in Table 2.
Triglyceride (Table 4). After 5 days on the experimental diets containing sunflower seed oil
there was a significant decrease in the concentration of triglyceride in fasting serum but no
change while on the diets containing cream. The extent of the decrease was similar to that
found in the men except in the sunflower seed oil, fructose and starch diet where the decrease
was significantly greater in the women. The diets containing cream did not, after 5 days, alter
the triglyceride concentration during fasting women.
No significant difference was found in the response with the various dietary carbohydrates
used (Fig. 1).
Cholesterol (Table 4). As with the triglyceride and as found in the men, the diets containing
sunflower seed oil resulted, after 4 and 5 days, in a significant decrease in the cholesterol
concentration of serum during fasting. The extent of the decrease was similar in both women
and men. There was no difference in response between fructose and glucose or between starch
and glucose (Fig. 2).
Phospholipid (Table 4). Again, as in the other lipid fractions and as found in men, the concentration of phospholipid decreased after 4 and 5 days on diets containing sunflower seed oil.
No difference was found between the carbohydrates in causing this effect (Fig. 3).
DISCUSSION
The proportions of carbohydrates, fats and proteins used in these experimental diets are similar
to those normally consumed and are therefore more physiological than experimental diets
containing excessive proportions of one constituent, and are therefore more relevant to normal
circumstances than some of the diets we have used before.
Using the design of experiment reported here it is possible to uncover the influence that one
dietary food group may have on another, and it is also possible to learn of small differences
that may exist between one type of carbohydrate and another, differences which may be masked
by the effects of other and more powerful influences. Thus the finding that in men starch results
Fats, carbohydrates and serum lipids
273
in a serum triglyceride concentration after fasting that is higher than when glucose replaces
the starch, that the serum cholesterol concentration is about 10% higher after a 5 day diet with
fructose than with glucose and that with cream in the diet the phospholipid concentration is
greater with glucose than with thermally equivalent amounts of fructose, are differences that
could be masked by the presence of other constituents of the diet. These differenceswere small
under our conditions, but the mechanism underlying them might be of significancein long-term
consumption. For example, sunflower seed oil lowers the serum cholesterol concentration, as
is widely recognized, but the extent of the lowering is 10% greater when the diet contains
glucose rather than fructose.
There are various contradictory reports about the effects of carbohydrates, especially
sucrose, on the concentration of lipids in serum of fasting subjects (Antar & Ohlson, 1965;
Dunnigan, Fife, McKiddie & Crosbie, 1970; Kuo, 1969; Macdonald & Braithwaite, 1964;
Porte, Biermann & Bagdade, 1966). In view of the findings reported here, one explanation for
these apparent contradictions could be that the nature of the constituents of the diet other than
the carbohydrate might have masked the effect under investigation, even though that effect
was present. Thus it seems that dietary fructose is associated in men, in the short term, with
higher concentrations of serum triglyceride during fasting than is glucose. This difference is
not immediately apparent when sunflower seed oil accompanies these two carbohydrates, but
is present, even though the effect of sunflower seed oil on triglyceride concentration in serum
of fasting subjects is more striking.
The ability of sunflower seed oil to lower the concentration not only of cholesterol but of
triglycerides and phospholipids would suggest that the effect of this polyunsaturated fat is on
metabolism rather than absorption. It is possible in these experiments, however, that as cream
contains cholesterol, the decrease in serum cholesterol in the sunflower seed oil diets may be
due to the cholesterol-free nature of the diet.
The effect of the type of dietary fat on the concentration of lipids in serum of fasting subjects
does not seem to be dependent on the sex of the consumer, whereas the lipid response to
fructose does depend on the sex of the consumer, confirmation of previous findings (Macdonald,
1965).
The triglyceride in the serum after a fast of at least 12 h is probably endogenous though no
lipoprotein analysis was performed to coniirm the absence of chylomicrons. If exogenous lipid,
as chylomicrons, had been present in any quantity, the serum triglyceride concentration after
fasting would have increased and not, as was found, decreased by about 20% after 5 days on the
diet containing sunflower seed oil.
As endogenous serum triglyceride is mainly synthesized in the liver, using free fatty acids as
the fatty acid source in the fasting state, it is difficult to understand how dietary triglyceride can
interfere in this synthesis and also how the extent of synthesis can be modified by the nature of
the dietary fat. The sunflower seed oil must presumably either accelerate the removal of endogenous triglyceride or decrease its rate of formation, directly or indirectly. Removal of serum
triglyceride is largely under the influence of lipoprotein lipase and the activity of this enzyme
may be affected by the composition of exogenous lipid (Pawar & Tidwell, 1968).
Perhaps the concept that endogenous triglycerides are mainly influenced by dietary carbohydrate has arisen from studies in which the diet has contained little polyunsaturated fat. It
seems that, in diets containing relatively little polyunsaturated fat, carbohydrate is the major
influence affecting the endogenous triglyceride concentration after a 12-14 h fast, but this
274
I. Macdonald
effect of carbohydrate can, it seems, be masked by the action of sunflower seed oil. The fasting
triglyceride concentration may possibly be determined by the ratio: amount and type of dietary
carbohydrate/amount and type of dietary fat.
ACKNOWLEDGMENTS
I am very grateful to the volunteers, and to Beecham Products for a grant.
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