DIET AND BLOOD CHOLESTEROL IN NORMAL WOMEN* · 2003. 3. 12. · cholesterol which we had previously...
12
DIET AND BLOOD CHOLESTEROL IN NORMAL WOMEN* BY RUTH OKEY AND DOROTHY STEWART (From the Laboratory of Household Science, University of California, Berkeley) (Received for publication, November 29, 1932) That t,he long continued feeding of diets rich or poor in fat has a definite effect upon the general level of blood lipid has been indi- cated by data on dogs recently published by Bloor (1). If we may assume that concentration of blood cholesterol in any way affects the deposition or accumulation of sterol in the tissues, we have reason to be concerned with the factors which affect the extreme variability of blood cholesterol level in human beings, and especially in women. The purpose of the study here reported was 2-fold: (a) to gain some evidence of the effect in human beings of continued feeding of cholesterol-rich food upon postabsorptive values for blood cholesterol, and (b) to see if the monthly variations in blood cholesterol which we had previously observed (2) in normal wo- men were affected by cholesterol intake. Our plan called for an intensive study of a few subjects on diets of variable cholesterol cont,ent, but of quite a usual character. The first or control diet,* of constant and rather low fat as well as * Presented before the meeting of the American Society of Biological Chemists at Philadelphia, April, 1932. 1 Detailed Description of Diets. Diet Z-This was a control diet which con- tained orange juice 230 gm., whole wheat bread 160 gm., butter 52 gm., jam 13 gm., lettuce 130 gm., lamb chops 92 gm., cream 26 gm., milk (1 pint) 467 gm., mayonnaise 13 gm., wheat germ 20 gm., potato 120 gm., two servings of vegetable of approximately 100 gm. each per day, and two of fresh fruit, usually apples. Diet I, the low cholesterol diet, contained, as far as we could ascertain from published data and from our own analyses, in cases where figures were not available, 0.77 gm. of cholesterol per day. Diet II-This high cholesterol diet contained the yolks of four eggs (64 pm.) daily and on alternate days 2 pound (118 gm.) of liver was substi- tuted for the lamb chops. The cholesterol content of this diet was calcu- 717 by guest on December 7, 2020 http://www.jbc.org/ Downloaded from
Transcript of DIET AND BLOOD CHOLESTEROL IN NORMAL WOMEN* · 2003. 3. 12. · cholesterol which we had previously...
DIET AND BLOOD CHOLESTEROL IN NORMAL WOMEN*
BY RUTH OKEY AND DOROTHY STEWART
(From the Laboratory of Household Science, University of California, Berkeley)
(Received for publication, November 29, 1932)
That t,he long continued feeding of diets rich or poor in fat has a definite effect upon the general level of blood lipid has been indi- cated by data on dogs recently published by Bloor (1). If we may assume that concentration of blood cholesterol in any way affects the deposition or accumulation of sterol in the tissues, we have reason to be concerned with the factors which affect the extreme variability of blood cholesterol level in human beings, and especially in women.
The purpose of the study here reported was 2-fold: (a) to gain some evidence of the effect in human beings of continued feeding of cholesterol-rich food upon postabsorptive values for blood cholesterol, and (b) to see if the monthly variations in blood cholesterol which we had previously observed (2) in normal wo- men were affected by cholesterol intake.
Our plan called for an intensive study of a few subjects on diets of variable cholesterol cont,ent, but of quite a usual character. The first or control diet,* of constant and rather low fat as well as
* Presented before the meeting of the American Society of Biological Chemists at Philadelphia, April, 1932.
1 Detailed Description of Diets. Diet Z-This was a control diet which con- tained orange juice 230 gm., whole wheat bread 160 gm., butter 52 gm., jam 13 gm., lettuce 130 gm., lamb chops 92 gm., cream 26 gm., milk (1 pint) 467 gm., mayonnaise 13 gm., wheat germ 20 gm., potato 120 gm., two servings of vegetable of approximately 100 gm. each per day, and two of fresh fruit, usually apples. Diet I, the low cholesterol diet, contained, as far as we could ascertain from published data and from our own analyses, in cases where figures were not available, 0.77 gm. of cholesterol per day.
Diet II-This high cholesterol diet contained the yolks of four eggs (64 pm.) daily and on alternate days 2 pound (118 gm.) of liver was substi- tuted for the lamb chops. The cholesterol content of this diet was calcu-
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718 Diet and Blood Cholesterol
sterol content, was given for 4 or 5 weeks (one full monthly cycle). A few weeks respite from this routine were allowed and then the so called high cholesterol regimen (Diet II) was instituted. This. consisted essent,ially of the same basal diet given before with egg yolk and liver added to bring the cholesterol content to 3.1 gm. daily and was continued for a similar period. Finally, after a break in the monotony of the regimen had again been allowed, the menstrual and intermenstrual response of these same subjects on the same basal diets to the ingestion of cholesterol as such was studied (Diet III). Unfortunately the latter period of observa- tion had to be shortened because of the close of the school year.
Four normal women, all senior or graduate students in nutri- t.ion, served as subjects. Blood samples were taken before break- fast and at very nearly the same time in the morning three times a week; occasionally more frequent samples were taken at or near the time of onset of menstruation. The general technique de- scribed in previous papers of this series was followed.
Blood samples were measured immediately into alcohol-ether and filtrates prepared according to the technique of Bloor, Pelkan, and Allen (3). Total and free cholesterols were determined in the whole blood filtrates by precipitation and oxidation of the digito- nide according to the method previously described by one of us (4). The modification of the procedure introduced by Yasuda (5) was adopted only in so far as the acetone washing of the digito- nide was concerned. We should perhaps state that we have found it relatively easy to get dependable recovery of added cholesterol with asbestos filters when t.he concentrations in the samples lie within the ranges covered by normal bloods.
The determinations were made with whole blood-partly be- cause we wished to avoid taking the larger samples necessary for plasma determinations; partly, however, because we are convinced that much error may be introduced into plasma cholesterol deter-
lated as 3.1 gm. Amounts of bread and potato, vegetables, and fruit were omitted from this diet to make the caloric content approximately equal to that of Diet I without altering the fat and sterol content.
Diet Ill-This n-as a basal diet, essentially the same as Diet I, to which cholesterol was added (in the butter) to make the total content approxi- mately equal to that of Diet II, i.e. 3 gm. This diet differed from Diet II in that the eggs and liver were omitted.
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R. Okey and D. Stewart 719
mination by variations in the distribution between plasma and corpuscles due to slight variations in concentration and conse- quently osmotic pressure introduced by the anticoagulant (pos- sibly an indirect effect on emulsification) and by day to day varia- tions in temperature and speed of centrifugation in the separation of the plasma. We wish, however, to reserve further comment on this phase of the subject until we have accumulated more data, and mention the point at this time only because of certain state- ments with regard to the use of plasma for cholesterol determina- t.ions in the recent literature. Det’ailed data are given in Table I, while mean results are summarized in Table II.
DISCUSSION
The question of relationship of diet to blood cholesterol is one on which the conflicting evidence in the literature can to some extent be accounted for by variations in conditions of experimenta- tion, pathology of subjects used, and failure to appreciate limita- tions of the methods employed. In general the results of short time experiments are inconclusive. Bruger and Somach (6) have recently stressed the extent of diurnal variations in blood cholesterol, even in normal subjects. They conclude from data covering in each case observations taken at 2 hour intervals for from 4 to 24 hours that the ingestion of food has no appreciable effect, either early or late. Close examination of their figures shows, however, that all the cases studied after ingestion of food were pathological, and certain of their figures suggest the pos- sibility of other interpretations, notably the effect of water inges- tion or of progressive loss of water during fasting.
A number of papers dealing with the effect of single ingestions of cholesterol or cholesterol-rich foods present equally unsatisfac- tory data.
In a recent paper by Hunt (7) the literature on the subject is reviewed in connection wit,h diabetes. Her conclusion from her own data is characteristic; i.e., she states that egg-eating diabetics do not necessarily have high blood cholesterol values, but in the one case with high cholesterol from whose diet eggs were omitted, there was a real drop in the blood cholesterol level.
Myassnikow (8) got no measurable effect on blood cholesterol in normal subjects by a single feeding of eight eggs or in three
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TABL
E I
G
Chole
sterol
in
Bl
ood
Follo
wing
Di
ets
of V
aryin
g Ch
oleste
rol
Cont
ent
0
Tota
l an
d fre
e ch
oles
tero
l ar
e m
easu
red
in
mg.
pe
r 10
0 cc
. of
blo
od;
este
r ch
oles
tero
l is
mea
sure
d in
bo
thm
g.
per
100
cc.
of
blood
an
d pe
r ce
nt
of
tota
l.
Diet
I,
low
chol
este
rol
Subje
ct E-
Tu
/ Su
bject
M-T
u ]
Subje
ct M
-Hj
I Su
bject
G-HI
Date*
I-
-3
-1
$1
+2
$4
$6
$9
$11
+13
-12
-10 -8
-5
‘1 -
-
Chole
sterol
I
rota
1 FW
-
190
88
167
89
154
82
149
92
156
109
168
90
152
102
152
92
160
104
201.
79
17
7.
91
179
LO4
154
92
-
~ Da
te*
Ester
__
____
Per
cent
.0
3 54
.7
-1
78
46.6
0
73
47.4
+1
56
37
.6
$3
47
30.1
$5
77
45
.8
$8
50
32.8
+lO
60
39
.4
+13
56
38.7
-1
3 .2
2t60
.6
-11
8614
8.5
-8
75
41.8
-6
62
40
.2
-4
-
Chole
sterol
I
:ota
1
177
173
152
158
145
149
149
137
137
149
158
136
151
Date’
he
ES
& -~
__
Per
cent
10
2 ‘7
5 42
.3
-4
98
75
43.4
-2
89
6341
.4
0 91
67
42
.4
+2
107
38
26.2
+5
94
55
36
.9
f7
95
54
36.2
+9
82
56
40
.8
+12
98
40
29.1
+1
4 84
65
43
.6
-11
95
63
39.2
-8
92
43
31
.6
-6
89
62
41.0
-4
-2
-1
0
Chole
sterol
I
- ‘1 -
- -
k&al
Fret
-- 149
105
147
97
151
100
151
100
145t
91
. 16
61
94,
1511
85
, 18
3t
95,
151
82
151
102
156
103
173
106
190
113
147
97
168
98
162
72
___
Date’
Es
ter l
I Pe
r ce
nt
- I.
43
28.8
+l
50
34.0
$3
51
33
.7
f6
51
33.7
$8
54
t 37
.2
+10
72t4
3.3
-13
66t4
3.7
-12
88t
48.0
-1
0 69
45
.6
-7
49
32.4
-6
53
33
.9
-5
67
38.7
-4
77
40
.5
-3
50
34.0
0
70
41.6
+l
90
55
.5
rota1
Chole
sterol
u 5;’
FW
3 Es
ter
e-
143
149
141
149
147
126
138
128
160
168
145
132
162
137
154
85
58
40.5
w
83
66
40.4
r
91
50
35.4
&
86
63
42.2
73
73
49.6
0
82
44
34.8
F
77
61
44.1
r
77
51
39.6
!t
97
63
39.3
2
90
77
45.8
-
94
51
35.1
92
40
30
.3
94
68
41.9
96
41
25
.4
106
48
31.1
-
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Diet
II,
hi
gh
chol
este
rol
Diet
III
, ad
ded
cho-
le
ster
ol
-14
-12
-10 -7
-5
-3
0
+2
$4
+7
+g
-1
$1
+2
$3
+4
-3
-2
-1 0
$2
$10
+11
+12
fl3
+15
169
184
168
183
186
168
166
173
182
168
158
143
143
145
156
159
162
152
158
143
151
169
173
162
168
148
99
01
07
10
93
91
89
89
12
08
08
78
94
90
88
86
- 89
89
89
90
93
83
00
91
88
91
-
71
42.0
-1
2 84
45
.6
-10
61
36.3
-8
73
39
.3
-5
93
50.0
-3
76
45
.2
-1
77
46.3
+l
85
49
.2
+2
70
38.4
f4
60
35
.7
+6
50
31.6
+9
65
45
.4
+ll
49
34.2
+1
3 55
37
.9
416
69
44.2
63
39
.5
-- __
72
44.4
64
42
.0
69
43.0
53
37
.1
57
37.7
86
50
.8
73
42.1
71
43
.8
80
47.0
57
38
.4
158
158
162
162
154
173
169
184
171
184
179
168
177
173
8i 8f
88
9:
9:
lO(
104 88
11
: 9f
10: 91
1o
C 11
:
- -
71
4 72
4
74
4 69
4
61
3 73
4
65
3 96
5
59
3 87
4
77
4 76
4
77
4 58
3 :4
.3
-1
:5.6
+l
5.
5 +3
.2
.5
$6
t9.G
$8
2.2
-+lO
‘9
.0
-12
2.2
-10
84.5
-8
.6
.2
-5
.3.0
-3
5.
2 -1
3.
5 0
,3.5
$1
179
169
175
186
1 19
0 1
188
1 18
4 1
171
168
1 18
4 I
179
1 20
0 1
180
181
1 94
96
94
13
13
10
10
99
12
22
11
10
97
.Ol
85
47.5
1 -1
73
43
.2
+l
81
46.2
f4
73
39
.2
+6
77
40.5
+s
78
41
.4
+ll
74
40.2
-1
0 72
42
.1
-8
56
33.3
-7
62
33
.6
-5
68
38.5
-3
90
45
.0
0 83
46
.1
+2
80
44.1
-J
r4
-__
-9
-8 -3
-2
-1 0
+1
$2
$3
- -
- --_
_ 14
7 1 0
0 47
31
.9
-2
154
1 02
53
34.4
-1
17
7 99
78
44
.0
0 17
7 98
79
45
.0
+1
160
98
62
38.7
+3
15
9 91
68
42
.7
3-11
16
4 94
70
42
.6
+12
168
97
71
42.2
+1
3 16
6 97
69
40
.9
f14
- -
- -
139
154
188
173
162
154
154
154
149
149
156
149
152
139
135
147
154
160
171
152
158
158
162
88
52
37.4
93
61
37
.7
95
93
49.4
11
5 58
33
.5
82
80
49.1
89
66
42
.8
91
63
40.9
10
5 49
31
.8
86
63
42.0
93
56
36
.2
gj
* 87
69
44
.2
0
83
66
44.2
ir
88
65
49.4
Y
-_-
tj 88
47
34
.8
m
90
57
38.7
$
90
64
41.5
8
100
60
37.5
$
107
64
37.4
cc
89
63
41
.4
92
66
41.7
91
67
42
.4
94
68
41.9
* Th
e da
y of
th
e on
set
of
men
strua
tion
is r
ecor
ded
as 0
; da
ys
prec
eding
th
e on
set
of
men
strua
tion
as
(-);
and
days
fo
l- lo
wing
it
as
(+).
2 w
7 Sa
mpl
es
take
n wh
en
the
subj
ects
we
re
suffe
ring
from
sli
ght
cold
s.
,, ,,
,,,
,, /,
8, I/
r 8,.
,“/
,
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TABL
E II
Wan
Bl
ood
Chol
este
rol
Valu
es
The
resu
lts
are
expr
esse
d in
mg.
pe
r 10
0 cc
. of
blo
od.
Subje
ct
E-T
u ...
......
......
...
M-T
u ...
......
......
...
M-H
j ...
......
......
...
G-H
j ....
......
......
..
Mea
n fo
r di
et
......
.. St
anda
rd
devi
atio
n.
P.e.
of
mea
n.
......
..
Mean
tot
al ch
oleste
rol
I Fr
ee
chole
sterol
I
Ester
ch
oleste
rol
Diet
I I
I Di
et II
P.e.
P.e.
P.e.
P.e.
----
---- 16
2 f2
.3
165z
U.6
162
f2.3
16
5zU.
6 15
1 f2
.3
169f
1.6
151
f2.3
16
9f1.
6 15
8 f2
.2
181z
lY1.
7 15
8 f2
.2
181z
lY1.
7 14
5 f2
.2
155f
2.2
145
f2.2
15
5f2.
2
154.
0 7.
5 2.
9
Diet
III
Diet
I Di
et II
Diet
III
Diet
I Di
et II
~___
____
P.9.
P.e.
P.e.
P.e.
P.e.
P.e.
_-_-
----_
_---
159f
1.6
95
f1.7
96
11
.7
90
~0.9
67
z1
~3.3
69
~2
.1
93
f1.3
97
,=!
A.6
58
f2.5
73
f1
.9
164f
2.1
98
z!z2
.110
6 51
.6
96
10.7
62
f2
.1
75
f1.6
15
5f2.
2 88
f1
.4
92
~1.9
93
rt1
.3
57
f1.9
64
~2
.2
159.
3 93
.5
60.6
5.
1 4.
9 3.
5 2.
4 1.
9 1.
4
Diet
III P.e.
~- 68
f2
.1
66
~2.4
62
f1
.4
65.0
3.
3 1.
6
Prob
able
er
rors
of
mea
ns
are
com
pute
d by
the
for
mul
a p.
e.
of m
ean
= 0.
6745
n/G
wh
ere
CJ =
d/
Z(@
)/n
- 1.
Fi
gure
s re
pres
entin
g va
lues
ta
ken
when
th
e su
bjec
ts
were
su
fferin
g fro
m
cold
s ar
e om
itted
in
co
mpu
ting
mea
ns
and
prob
able
er
ror
of m
eans
.
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R. Okey and D. Stewart 723
subjects by feeding eggs fol a 4 day period. In one case of cirrho- sis of the liver, however, he secured a tremendous rise in blood cholesterol level as a result of feeding eggs.
The differences in response to fat feeding, which were ascribed by Rony and Ching (9) to the previous state of nutrition of the experimental animal, together with the work of White and Hunt (10) who found that blood cholesterol values were distinctly higher in overnourished than in normal children, suggest one explana- tion of differences in response to diet in short time experiments. This effect of previous state of nutrition is also in keeping with the findings of Page and Menschick (11) who found (from balance experiments and tissue analyses in rabbits) that cholesterol tended to accumulate in the tissues of rabbits other than brain after feeding excessive amounts of cholesterol. They believe that their data establish ability of the rabbits to destroy cholesterol in limited quantity and their figures support the conclusion that when cholesterol is absorbed an equilibrium is set up between cholesterol in food, tissues, and excreta which with high cholesterol intake results in deposition of cholesterol in tissues.
The literature on response of blood cholesterol to fat feeding has recently been so well reviewed by Bloor (1) that this aspect of the problem need not be considered here. As stated above, Bloor’s own data indicate that the general level of blood cholesterol in dogs 14 hours after the last meal is affected by fat intake. The rela- tionship of this higher level of blood cholesterol to cholesterol deposition in tissues or from bile is a subject calling for further study of laboratory animals.
Our own data, as will be seen from the summary in Table II, indicate that the feeding of the cholesterol represented by a moderate number of egg yolks tends to produce a consistent, if slight, rise in the mean postabsorptive level of blood cholesterol in normal women. The less marked, or doubtful, indication of response to the feeding of cholesterol as such in butter may be due to the smaller number of blood samples from the period on the last named diet, or more probably, to a difference in absorption of the cholesterol. The intimate mixture of lecithin or lecitho- protein, fat, and cholesterol in egg yolk is not strictly comparable to crystalline cholesterol, which probably does not even stay in solution in butter fat throughout the alimentary tract. That
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724 Diet and Blood Cholesterol
the effect of egg yolk as such is a question of considerable impor- tance is evidenced by the increasing number of reports of develop- ment of arteriosclerosis in comparatively young diabetics inci- dent to the recent use of high fat diets containing, as a rule, many eggs in the treatment of that disease.
The mean percentage of esterified cholesterol was slightly higher, i.e. 41.9 and 41.5 per cent, respectively, on egg yolk and on cho- lesterol as such than on the control diet, i.e. 39.4 per cent, probably not a great enough variation to be significant. But it is at least interesting to note that Bloor found a larger variation in the same direction in dogs on high fat diets, but not in rabbits on similar diets.
In general our observations of the mean peroentages of esteri- fied cholesterol in the blood of normal young women have given considerably lower figures than those found by Bloor in dogs. The mean values for a previous series of approximately 150 ob- servations in this laborat,ory in which the calorimetric method was used with bloods of women on uncontrolled diets, were 43 per cent ester. The percentages of esterified cholesterol observed by Kaufmann and Mtihlbock (12) in postabsorptive blood samples are sometimes in good agreement with those we have found. Sometimes, however, their subjects show a considerably higher percentage of ester. This may be due to differences in dietaries in Berlin and in California.
The degree of variability of blood cholesterol at the time of onset of menstruation does not appear to be greatly affected by a varia- tion in cholesterol intake of the extent used in this study. Neither the data reported in this paper nor the unpublished data on un- controlled diets, however, substantiate the earlier stat.ement of Kaufmann and Miihlbock (13) to the effect that the menstrual drop in blood cholesterol is almost entirely a drop in free choles- terol. Both fractions seem to be involved; in some cases to an almost equal extent and in some cases the ester varies to a greater extent than the free cholesterol. The figures do suggest that the menstrual fall in ester is followed first by an increase in the free cholesterol, and then more slowly, by an increase in the ester fract,ion. This was true in even greater degree of the menstrual variations in ester cholesterol in some of our subjects on uncon- trolled diets. It seems probable that free cholesterol is mobilized for some definite purpose during the menstrual period.
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R. Okey and D. Stewart 725
Dahlmos and Sole (14) and Degkwitz (15) have pointed out that cholesterol acts in the blood as a lyophobic colloid, while lecithin, as a lyophilic colloid has an antagonistic effect on mem- brane equilibrium. Our previous findings (2) indicate that the postabsorptive level of blood lecithin remains very nearly con- stant during the menstruation but that total fatty acid increases somewhat at about the time of the greatest fall in blood choles- terol. The investigators noted above found that when choles- terol was injected into the blood stream there was a hydremia with increased chloride in blood and urine, while injection of lecithin produced the opposite effect, i.e. imbibition of water by tissue with a decreased amount of water and chloride in the blood stream. This would suggest that variations in proportion of lecithin to cholesterol in the blood stream, such as we have ob- served during the menstrual period, may be associated with surface tension variations resulting in alterations in capillary permeability, and in tissue imbibition of water.
It has been impossible for us, with subjects who are actively engaged in college work, to make complete water balance experi- ments during menstruation. We have, however, kept daily weight records for some twenty students for periods of 1 month each. In approximately three-fourths of these there was no significant weight variation at the time of menstruation, but in the others there was a gain of 1 to 3 pounds shortly before the onset of menstruation with a sharp fall when menstruation began. And, interestingly enough, the students who showed the gain in weight almost all had histories of menstrual headaches or discomfort. Blood chloride determinations made in this labora- tory on twelve subjects at 3 day intervals for 1 month (unpub- lished data, Okey and Foges) show a slight menstrual variation in postabsorptive blood chloride level in five cases only. The degree of variation is in the direction to be expected, but so small as to be statistically insignificant. Again, however, the varia- tion was observed in the cases with the history of greatest men- strual discomfort.
All of this suggests the interesting possibility that menstrual congestion may be due to a water imbibition mechanism which results in increased tissue retention of water just before the onset of menstrua,tion; and that t’his may in turn be due to a variation
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726 Diet and Blood Cholesterol
in lipid ratios in blood and tissue. Our data are insufficient to justify a more definite statement. We feel, however, that the data here given indicate that, within the limits of the amounts 60 be found in the ordinary diet, cholesterol feeding has little effect on the menstrual variations.
SUMMARY
Data for free and total cholesterol of whole blood samples taken three times weekly are reported for four normal women who were placed successively, for periods of approximately 1 month each, on (1) a constant diet low in cholesterol, (2) ‘one containing a moderate amount of cholesterol in egg yolk and liver, and (3) a diet low in food cholesterol to which a like amount of cholesterol as such was added.
The mean values for the month for both tot.al and free choles- terol were consistently somewhat higher than for the control diet both when the diet containing egg yolk was given and when choles- terol as such was added to the control diet, but the diet containing the egg yolk produced the greater effect. Percentage of esterified cholesterol became slightly higher with increased cholesterol intake. The bearing of these findings upon the et,iology of cer- tain pathological conditions developing in patients fed therapeutic diets rich in egg yolk is discussed briefly.
The higher level of cholesterol intake was found to have very little, if any, effect upon menstrual variations in blood cholesterol in these particular subjects. A possible relationship between variations in lipid ratios in blood and tissues and the imbibition mechanism which produces menstrual congestion is suggested.
We are indebted to the Research Board of the University of California for funds which made this work possible.
BIBLIOGRAPHY
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Ruth Okey and Dorothy StewartNORMAL WOMEN
DIET AND BLOOD CHOLESTEROL IN
1933, 99:717-727.J. Biol. Chem.
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