.-l therosclerosis Elscvier Publishing
Company,
137
-4msterdam - Printed in The Netherlands
Review
SUGAR
INTAKE
AND
CORONARY
HEART
DISEASE
SCMMARY
In order to incriminate coronary
heart
disease
data on sugar intake
factors.
incidence
circumstances
is specifically
associated
(4) Information
of contexts.
does not significantly aetiology
of CHD,
crimination minority
the lowering of sugar intake,
of the metabolic
sugar. Secondly,
is possible.
groups in Western
whether,
Thirdly,
populations
Epidenziology - I~zdin
that
or voluntarily, risk
which deal with sugar and
and the following conclusions such evidence
as is available
bearing in mind the multifactorial within
more
a given context,
intensive
research
- Lipids - Myocardial
major
in-
on particular
might provide more trustworthy
Cigarette smokiu, u - Covonavy head disease (CHD)
Key words:
data
sequelae.
it is questionable
of sugar
demonstration
animals to sugar in a variety
mechanisms
evidence is incomplete,
incriminate
(2) Corresponding
involuntarily
of
(1) Accurate
of CHD or its associated
on the response of experimental
although
are needed:
rate. (3) Unequivocal
has been made of these aspects
Firstly,
of sugar in the causation
of evidence
and in sub-groups.
or mortality
and pathological
An examination were reached.
types
with a fall in the frequency
(5) Knowledge
their physiological
consumption
several
in total populations
on CHD prevalence, in propitious
excessive
(CHD),
inferences.
- Dietary habits -
iplfnvctiou - Ovemutvitio~~
- Racial differences - Stavch - Sucvosr*
INTRODUCTIOi'i
Opinions about the causation who believe
that
diet is almost
of coronary irrelevant,
heart disease (CHD) range from those like CAMPBELL~
and
=Ithr?vosclerosis,
ROBB-SMITHY,
to
1971, 14: 137-152
A. R. P. WALKER
138 those who assert that majority,
of CHD4-11. sumption intake,
diet is wholly responsible,
of course, are convinced Increases
in its prevalence
of a number
of dietary
responsibility
aetiology
difficulties,
promotive
foodstuff
is retarded?
aetiological
importance
specific incriminatory
(b) random
or nutrient
Since
such as ethnic
components
voluntarily
practices,
on the prevalence
(4) The response (5) The metabolic
that
groups,
~‘.g.
class,
religion,
prevailing,
etc.
demonstrates
involuntarily
that,
if
(from war, prison,
or
this will be followed by a fall in
risk factors,
provided, of course, that the are not too old.
to sugar, there must. as a beginning, given in (1) and (2). Satisfactory
be a significant evidence in (3),
In addition,
it would be
of,
of experimental mechanisms
animals
to sugar in a variety
of contexts.
which deal with sugar and its physiological
or
sequelae.
PRECISE
KNOWLEDGE
ALENCE
OR MORTALITY
Atherosclerosis,
social
unequivocally
whether
(as in field trials),
The first two requirements
Agriculture
of evidence.
of, and/or the mortality
and that the persons involved
to have knowledge
Sugar
a
listed.
of CHD or of its associated
between the information
DATA
to have
heart disease, also those whose diet is
of course, could even provide proof of specific implication.
(a)
and
in (a) total popu-
and (c) special population
or traditional
reduced,
For blame to be attached
pathological
CHD?
is reduced,
claimed
of sugar intake
degree of “westernization”
must be forthcoming
change in diet be susta’ned,
valuable
C,HD
will be made to learn to what extent
of populations,
precise data are required
or
of dietary
evidence of ischaemic
be substantially
the prevalence
to excess promotes
sugar, there are several requirements
from, CHD in the types of population
like conditions)
are beset
of non-dietary
eaten or when consumption
is a precise knowledge
samples
by factors
(3) Evidence
consumed
the latest
living in town or country,
sugar intake
in particular,
r81e can be accorded to this foodstuff.
those with and without
(2) Next,
caloric
and sugar. Is it
to assess the measure of
of the existence
is sugar, an attempt
(1) The first essential
correlation
animal protein,
must be adduced before it can be accepted
are habitually
In order to incriminate
modified
in the con-
apart from increased
rbles? Efforts
because
of the disease, what evidence
the disease
in the development
and possibly even racial 12J3. In view of the multifactorial
(2) that when small amounts
whether
fat, cholesterol,
primarily
environmental
(1) that a particular
lations,
These,
borne by diet in general, or by specific nutrients
by numerous risk factors,
their respective
et a1.3. The great
CLEAVE
have been linked with increases
components.
include total fat, saturated
possible to estimate
such as
that diet is strongly implicated
ON TOTAL
OF
will be discussed together.
SUGAR
INTAKE
IN POPULATION
AND
OF CORONARY
HEART
DISEASE
PREV-
GROUPS
POPULATIONS
consumption Organisation,
data
in different
sugar
1971, 14: 137-152
production
countries
are available
authorities,
and
from
the
Government
Vood
and
bodies.
SUGAR INTAKE ASD CORONARYHEART DISEASE
SUGAR
INTAKE
AND
CORONARY
HEART
DISEASE
cOZlMtY\’
Xemz sugar available g per capita per diem
Iknmarlc
139 137 136 134 134 133 120 118 113 91 88 72
Canada United Kingdom Xew Zealand Ilnited States Sctherlands Swcdcn Switzerland Finland Germany France Italy
Data
on intake
sumption
pev capita
(domestic
IN
as
139
WESTERN
POPULATIONS
CHLI (classification nzortalitv rate per 100,000 population ____~
420)
310 219 239 232 293 139 226 97 196 124 66 72
are arrived
and industrial)
at by dividing
the gross national
sugar con-
by the total
population; the result may be essay, pressed as consumption per di~z or per awuun. A moderately high consumption, 100 g or 3.6 oz sugar $ev diem equals 36.5 kg or 80.3 lb per anwm. CHD mortality data, crude and age specific, on the total populations of man) countries are available in World Health Organisation publications, also in Government health reports. Current representative
figures
on sugar
intake
and
CHD mortality
western countries, which have much the same age structure, from FAOI4 and WHO15 sources, and are given in Table 1. It will be observed
that
for most
western
countries
rate
in
have been obtained
listed
there
is a broad
association between sugar consumption and CHD. This was initially pointed out by YVUKIS~~. Data, however, are somewhat out of harmony in the cases of The Netherlands and Switzerland. Contributions somewhat similar to that of YLIDKIN~S, were made by OSASCOV.~ ct al.17 in Czechoslovakia, and ASHTONI~ m Britain, although the latter noted that in respect of the increased death rate from ischaemic heart disease, statistically, there was a closer association with total calories and fat consumed than with sugar consumption. A very important point is that several under-privileged populations have high intakes of sugar per caju’ta per diem, e. g. Brazil, 111 g, Columbia, 121 g, Costa Rica, 164 g, Nicaragua, 146 g, Uruguay, 109 g, and Mauritius, 103 g14. These high intakes are known to be valid from other sources. Yet the limited information available on these countries does not indicate that CHD is a serious public health problemlj+lg. From the foregoing information on total populations it is inferred that a high sugar intake is frequently associated with a high prevalence of CHD in most sophisticated, although not in some less sophisticated, populations. .~thevosczerosis, 1971, 14: 137-152
140
-4. R. P. WALKER
Factors
complicatiq Irrespective
described
has
(I)
iderpretatio?z
considerable
~Jncertainties
standable
of ?lational
data 0~1 sugar
of the measure of association to the heterogenicity
in respect of national
have ramifications
(2) There
Discrepancies
are discrepancies,
calculated
in patterns
between
as described,
series of households.
social classes.
and homehold
or real, between
In 1961, in the United
148M4
for example,
extensive
72 g sugar (purchased
than can be accounted
for by items not always included in household
reliability
of CHD
mortality
(i) the incidence follow-up,
(690,000
was reported inspection enquiries
and mortality Bantu,
as the primary
of other
surveys,
death
rate
or by
data
countries.
may
Thus, the
revealed a virtual identity
data for the respective
422,000
Caucasians)
between
given
countries.
combined
reduced the numbers
with
in 420)
men and 10 women.
in the certificates,
of the deceased,
In contrast,
in 1962, CHD (classification
cause of death in 27 Bantu
information
from relatives
as sugar), and to be far larger
data for CHD in the groups studied in their five year
and (ii) the mortality
Johannesburg
CHD
rates.
ap-
later.
but the problem is not serious in developed
recent studies of KEYS et al.21 in seven countries
when
studies in that
g, i.r. 64 g, appears
meals eaten away from home. This aspect will be mentioned Diflering
intakes.
the former
household
The difference,
(3)
such
from dietary surveys of large
Kingdom,
yielded a figure of about 84 g, namely,
wgar per capita
12 g from preservesso.
provide difficulties,
c.g.
Clearly,
OY individual
sugar available
and sugar intake as determined
proach gave a figure of 148 g $W diem 20. Yet, country
are under-
that are heterogeneous,
of diet and disease.
Izational,
apparent
There
of populatiom.
populations
composed of different ethnic groups or of very disparate differences
and CHD
the value of the approach
limitations.
due
reservations
idake
prevailing,
Yet
careful
dying probably
from
CHD to 6 men and 4 women22. Briefly
then,
in total
it is questionable
can be used for epidemiological
available per capita rate
populations,
in underprivileged
populations,
even
whether
data on sugar
purposes. Data on CHD mortality
under
propitious
circumstances,
are
unreliable. (b) DATA
ON RANDOM
Unfortunately,
no studies dealing specifically
on CHD prevalence although
SAMPLES OF POPULATIONS
no insuperable
consumption
practical
in households
by questionnaires with caution.
problems
or by individuals
are involved.
of sugar intake
inter- and intra-observer errors were thwarted
regarding
by resentment
during
periods
of hot weather
(affecting
in the community
Atherosclerosis, 1971, 14: 137-152
in seasons soft drink questioned.
of sugar
and may be elicited
however, of data,
attempts
in those questioned
we have noted that data obtained pattern
reproducibility
errors are small, although
theless,
Determination
is straightforward,
such as that of YUDKIN 23.The results,
In our experience
affect the intake
with the bearing
have been carried out on truly random samples of populations,
clearly
must be treated we believe
on further occasions. of home bottling
consumption)
that
to define such Never-
of fruit,
or
may markedly
The general validity
of the
SUGAR
INTAKE
data secured Working
AND
sugar consumption
Councils4 stated
report
described,
AND
electrocardiographic
for example,
that although
the
about
for protein,
by a WHO
used by groups
the making
of CHD in a random
sample
and electrocardiographic
Yet a major
BL4CKHuRN26.
criteria
preclude,
or incidence
can be based on clinical
using the procedures ROSE
of the
does not yield precise data, information
the prevalence
judgement
instances
Medical Research
questionnary
The recent
components.
In determining
by
is not in doubt.
is much more exact than that which can be obtained
fat, and other dietary
recently,
141
DISEASE
however,
of the British
of the dietary
population,
HEBRT
by these means,
Party
technique
CORONARY
Study
drawback
of workers
of satisfactory
group25,
or more
is that the different
prejudice,
comparisons
of
evidence,
and in many
of the occurrence
of
CHD”“. GROUPS (c) D .4TA ON SPECIAL POPULATION To incriminate the level of sugar intake
relation have
should
been
be apparent
undertaken.
in several
Some
others have been neglected.
in causing or promoting
types
population
of populations.
groups
The problem
have
attracted
may be approached
attention;
populations
with known differences
sugar intake differs, or aic~~ULYSIE.The following are groups, either which
vestigations tients
were those of
who had
disease,
or whose investigation
and compared
T.kBLE
YUDKIN
experienced
and then investigating
of myocardial
hfarctiort.
The initial
et al. 27738. They studied the sugar intake
either
to
would be likely to be rewarding.
Gro~$s with and without wideme
(1)
of CHD,
much
either by examining
what extent
have been studied,
of frequency
CHD, a cor-
Many investigations
myocardial
the figures obtained
infarction
or peripheral
in-
of pa-
vascular
with those of like series of persons out-
2
MEhN SU;GR All subjects
INTAKE
(g
pet’ &W)
IN
GROUPS
were males unless otherwise
WITH
AKD
WITHOUT
CORONARY
HEART
DISEASE
stated. -
Aztthors
Control groups 120.of
subjects
Ischaemic
heart diseascgroztps
_____-
we
(yews)
sugar illtake
120. qf subjects
age
(years)
sugar irdake
56 55.4 43-65 40055 under 60 under 60 44~58 under 60
77 78 117 96 69 65.2 79 96.9
20 20 20 66 100 50 170 80
56.4 55.4 42-64 40-55 under under 44-58 under
132 148 121 116 65.9 59.7 67.0 99.1
55.1 56.5 52.4
97.1 100.3 146.6
80 21 49
~UDKIN
AND
YUDKIN I’APP
RODDY3’
AND
MORLAND~~
et al.30
PlzuLet
al.31
FINEG~N
et al.32
FINEGAN
et al.33 (females)
HOWELL
AKD
BGRNS-COX
WILSON~~ et al.35
M.R.C. Studies24 Middlesex Hospital Hammersmith Hospital Scottish Hospitals
25 20 20 85 50 50 1158 160
160 21 94
54.4 56.4 53.2
.~therosclerosis,
60 60 60
100.1 103.5 167.1
1971, 14: 137-152
A. R. P. WALKER
142
wardly iree from these diseases. In two separate studies they found that men with myocardial be noted,
infarction ingested double the sugar intake of the control groups. It should however,
that
follow-up
studies
indicated
a smaller
difference.
Later,
were made by LITTLE et al. 29, PAPP et a1.30, PAUL et al.31, FINEGAN et
investigations
aZ.32133, HOWELL ANDWILSO~T34, BURSS-Cox et a1.35, ELWOOD et a1.37, and latterly, by a Working
Party of the Medical Research
Counci124. But all these workers de-
tected minor or no differences in sugar intake between the two types of groups. The conclusions
reached are most unlikely
to be vitiated
by the different criteria
in assessing ischaemic heart disease. The results obtained
are summarised
used
in Table 2.
The studies of BURNS-C• X et al.35 and of the Medical Research Council group24 are of special interest in that they employed
the same investigational
as were used by YUDKIN et a1.27328. BURNS-C• X et al.35 concluded of data now available to be a major
does not suggest that consumption
or specific factor in the production
Medical Research Council report24 concluded
procedures
“that the totality
of refined sugar is likely
of myocardial
infarction”.
The
that “the evidence in favour of a high
sugar intake as a major factor in the development
of myocardial
infarction
is extre-
mely slender”. While
the foregoing
investigations
primarily
concerned
the sugar intake
CHD, ELWOOD et al. studied sugar consumption
adult males with and without
ischaemic heart disease in a community37.
of and
In the male series, they found no evidence
that those with ischaemic heart disease had a higher sugar intake than the remainder; among women, those with angina had a slightly higher intake than the other women, although the difference was not significant There are two items epidemiological
(P > 0.05).
of less specific
studies at Bedford,
evidence.
KEEN AND ROSEN*, in their
found that the sugar intakes of “atheromatous”
men were not increased out of proportion
to their total caloric intake. In Glasgow,
BEGG et aZ.39 reported that their male group with arterial disease added significantly less sugar to their tea and coffee than their controls. An important cigarette
observation
habit was associated
was made by PAUL d al.31 who found with a greater intake of sugar,
revealed that the primary relationship
that the
and probit
analysis
was more likely to be between ischaemic heart
disease and cigarette consumption
rather than between ischaemic
sugar intake. The same conclusion
was reached by ELWOOD et al.37 and BENKETT et
aZ.36. In the former study, 89 g compared
mean sugar intakes in the Atomic
with 77 g per diem in the heavy and non-smoker
A further important
heart disease and
Energy
group were
groups, respectively.
point apparent from Table 2 is that the mean intakes of
sugar in the different
control
groups differed enormously;
this also applied
to the
groups with ischaemic
heart disease. Thus, the intake of the heart disease group in
the study of HOWELL AND WILSON~~ was 67 g per diem, whereas the corresponding figure in the Medical Research Council study at Glasgow and Edinburgh Yet at the latter centres, the daily sugar intake of the control far larger (with one exception)
than that of the heart disease groups in all the other
studies cited. This finding will be commented Atherosclerosis,
1971, 14: 137-152
was 167 g24.
group was 147 g, i.c.
on later.
SUGAR
INTAKE
(2) Britain,
AND
CORONARY
Grou~ps in western maintains
sume more than
HEART
143
DISEASE
co%?exts z&h
contrasting
that “many persons consume 150 g” per diem.
sugar
intake.
less than 45 g and very many con-
Consumption
by
vegans
is reported
a mean of 31 g has been given 41. Groups with high consumptions 118 g, and bus conductors,
carry
years,
accustomed
in locating,
(3)
investigations
Italian
D&me
group,
upon them.
respectively,
Incidence
would add to the value of the conclusions Caucasia?h
groups
et al.43 noted that the frequency studied.
say, two groups of 300 or more males of
to low or high sugar intakes,
out CHD prevalence
more meaningful,
itt westem
although
the respective the mortality
than that of other Caucasian+.
sugar
(J)
Grozips dl’feviq
New York,
consumptions
of Jews (Ashkenazi)
Our studies, however,
northern
about
were not
countries
g per diem, of total
Yet,
deaths
according
south of the cityas.
extent
Adventists47
than
to which this particular
was not reported. Indians
In Durban,
prevalence
in the average
U.S.A.
indicate
data,
is known
to be lower in
population,
although
the
group may have a lower than average intake of sugar South Africa,
according
are more prone to CHD than Hindu Indians;
the Transvaal
in the
due to CHD in the more prosperous
CHD
Seventh-Day
of groups of Caucasians
to death certificate
than in the poorer and industrial difSeeri?zg in religio~a.
this is not the
are higher than those investigated
(5)
Gro@s
group of approxi-
there appears to be little social
In “younger”
we have noted that the mean intakes
proportion
specifically
from CHD is far higher
have failed to reveal a signif-
In Britain,
class.
area, about SO-100 g $W dim45.
there is a greater north
in social
120-140
EPSTEIN
levelas.
in respect of sugar intakel6,“o.
case. In Johannesburg, in the south,
to
which are
group was double that of an
icantly higher sugar intake in a Jewish compared with a Caucasian mately the same socio-economic
and then
studies,
reached. In
contests.
of CHD in a Jewish
In Johannesburg,
class difference
to be low;
include bus drivers,
123 g42. Apart from the time, labour, and finance involved,
there should be no difficulty 60-69
in
YUDKIN40,
approximately
groups of the same socio-economic
equal intakes
status,
to death certificates,
Moslem
yet our studies on Indians
in
of sugar in Moslem and Hindu
such intakes
being of the order of 60-80
g
per diem45. (6)
Strict vegetarians
of refined cereals are usual@.
-
vegans.
31 g sugar per dienz41. Unfortunately, protagonists,
to investigate
that vegans have a relatively (7)
Town-co&r?/
differential
is almost invariably CHD mortality
low prevalence
there is only the impression
of C.HD@.
Several
investigations
have revealed
a marked
between urban and rural areas; that in the latter areas
lower. In Norway 50, for example, amounts
of sugar and
has been made, even by the relevant
in agriculture
was reported to be only a third of that obtaining
ly, the respective town-country
no attempt
this key type of population;
differences.
in CHD mortality
Among these people low intakes
One study, as already noted, revealed a mean intake of
of sugar consumed
difference in CHD mortality
of sugar intake in large centres of population
are not available.
obtains,
and fishing areas,
in Oslo; unfortunateIn the U.S.A.51,
yet there is insufficient
compared
with country .-IfhevoscZemis.
a
knowledge
areas. In respect 1971,
14: 137--152
144
A. R. P. WALKER
of regions in U.S.A.,
the mean intake
(from sugar and sweets) in the economically
superior and more densely populated north east, namely, 63 g per diemjs, is lower than that in the economically rate,
however,
poorer and more rural south, 73 g per d&253; CHD mortality
is higher
in the north-east
than
in the south
(excluding
the New
Orleans region)54. (8)
Grolb$s at d(fftwnt
problem state,
is to compare
levels
population
groups (i) in their primitive
with (ii) their urban more-developed
and the frequency usually
higher,
state.
sometimes
much higher,
have become a serious problem. to Indians
regard of unsophisticated in urban
This approach
Bantu
changes major
Little
in manner inadequacies
increases
with increases account
of knowledge
of several
in that
other
of appropriate them.
of CHD among
some puzzling points in the information on intakes
northern
Apart
from India. India,
of sugar simply as
in diet or of
Moreover,
there are
data have been reported
in
groups of subjects,
nor of the
from the foregoing,
there are
For example,
on relatively
in a major
poor subjects
study
subsisting
of sugar and fat far less than those usual in the west, CHD was stated
to be common In another
and have the same prevalence
study carried out in India,
correlated
with serum cholesterols*.
prevalence further
also in sophis-
or urban groups,
alterations
simultaneously.
no detailed
South Africa on sugar and cereal intakes
at Chandigarhs6,
in the consumption
in the sophisticated
associated undertaken
Africa,
in CHD55, have been interpreted
is taken
may
pursued by CLEAVE
with those in South
of life that have occurred
prevalences
and mortality
in rural areas compared with those partially
and also of refined cereals that have occurred cause and effect.
is usually low,
whereas in (ii) sugar intake is
has been actively
areas. The understandable
and which are associated
to the
or non-sophisticated
and CHD prevalence
in India compared
approach
In (i) sugar intake
of CHD may be low or negligible,
et al.3 in relation ticated
A popular
of sophisticatiolt.
as that found at Tecumseh,
dietary
particular
is required
U.S.A.57.
to be negatively
W’hile there is no doubt that, characteristically,
of CHD is higher in sophisticated
information
sugar was reported than in primitive
before allocations
populations,
of responsibility
much
may be made to
risk factors.
As just mentioned,
among populations
changes take place simultaneously; appreciated.
Thus,
in Britain
in various stages of transition,
their magnitude
about
a century
and significance
ago, the average
daily consumption
of bread made from lightly milled flour was about 600 gsa, moreover, a large amount
of oatmeal
porridge
was eatenso.
At present
numerous
are insufficiently among the poor
the consumption
of
bread in Britain
averages about 180 g prr
of fat in Britain
averages about 116 gso, the figure was 73 g in 190261, and about 53 g
in 186362. Further, contrasts figures
the current
die~rt
20.
Although present daily consumption
daily consumption
of sugar is about 84 gso, which
with the figure of about 60 g in 188162, and 25 g in 183562@. may
carbohydrate
not be fully representative,
Atherosclerosis,
are obvious.
supplied by bread has not only fallen considerably,
is now very largely the refined product. has risen,
the trends
the total
carbohydrate
1971, 14: 137-152
Although
intake
from
sugar consumption, bread
and
sugar
The
While these amount
of
but the foodstuff always refined, is much
lower
SUGAR INTAKE
AND CORONARY
now than in generations also their
interplay,
in importance
145
HEART DISEASE
past. These and other dietary
may
have
may be alterations
far reaching
changes which could be cited,
effects on the metabolism;
in the bulk-forming
capacity
not least
of the diet, with its
effects on lipid metabolisms*,6j. there
In respect of non-dietary changes likely to be relevant to CHD prevalence, has been a reduction in employment involving much physical activity. Of
importance already
too is the rise in frequency
referred
and intensity
to, can have an appreciable
bearing
of cigarette
smoking,
which, as
on sugar intake.
It will be apparent from the foregoing that the effects of changes in sugar intake tend to be confounded with the effects of changes, not only in intakes of other nutrients, but in other environmental factors. Clearly, support
in the investigations
a specific incrimination
THE EFFECT OF INVOLUXTARY
thus far described,
there is very little evidence
of sugar in the aetiology OR T’OLUNTARY
to
of CHD.
CHASGES IN SLTGARIXTAKE ON CORONARTI’
HEART DISEASE
-4s emphasized earlier the most crucial information required for the incrimination of sugar is evidence that when its intake is markedly reduced there is a fall in the prevalence
of CHD.
(1) War-time obsewatiom. In a number of countries, circumstances of war caused dietary restrictions which involved a reduction in sugar intake, and which were accompanied by a fall in mortality from CHD. However, as noted bv KEY+, other changes, dietary and non-dietary, occurred simultaneously. (2) Long-term co~@zemmt ia jm’sou. Usually, the sugar intake of prisoners is lower than that of the general population. There is some evidence, both in U.S.A.66,6i
and in South Africass, that serum cholesterol levels are lower, and CHD events are less frequent, under prison conditions. However, in prison, as during war-time, numerous other changes (in diet, activity, smoking, also emotional context) occur at the same time, which tend to confound interpretations.
Rtwlts offield trials. In man, although several large scale and protracted studies have been undertaken to determine the changes in CHD incidence that accompan> alterations in the dietary fat, no correspondingly large studies have been carried out using diets that differ only, or chiefly, in sugar intake. A major drawback is that even were such investigations carried out, then to vield worthwhile conclusions, regimens would have to be iso-caloric, for altered sugar intake with a concomitant change in weight would preclude firm conclusions. A fall in weight has been the rule rather than the exception 5n most of the prospective diet-CHD studies so far undertaken. For example, in the U.S.A. National Diet-Heart Studyss, the dietary changes that were associated with a fall in serum cholesterol level were also linked with .~thevosclerosis, 1971, 14: 137-1.52
146
A. R. P. WALKER
decrease in body weight, no long-term pursued.
diastolic
blood pressure,
The results disagree.
dietsTO-77. Such
changes
four reports
patients.
serum lipids were
however,
To illustrate
either
were slight
et ~1.88-90 at Toronto
between
Some
the scope of investigations
recently
described
kinds of dietary carbohydrate
studies
(period
15 days)
with
investigations
diets
showed that sucrose had no uniform
(period 4 weeks) with diets high in saturated
other
studies
a synergic
effect
the latter
studies,
between
dietary
however,
sucrose
and animal
were very high, supplying
et u1.86,91 found that high and low sucrose regimens serum cholesterol
as subjects,
that
or phospholipid.
of those
induced
hyperinsulinism”.
They
vascular
disease compared
with controls
significantly
greater
that in only a proportion heart
disease.
experiments
Their
periods
on the
insulin
of individuals those
to the alteration emphasized responses
in intake
out observations their
over a relatively
daily sucrose
tryglycerides
intake
averaged
These
workers
the need for further
the patients
therefore
concluded
of the remainder
full blame for the change
In this respect,
diets.
In the
experienced
attaching
on the
BIERMAN AND PORTEg2 have of insulin and triglyceride
(iii) In Cape Town, MANN et al.77 carried
long period of time, 22 weeks. Volunteers
reduced
information of starch
altered
4% less than before.
serum The
with a loss in weight. These workers on the epidemiology
and sucrose,
by the substitution
of serum trigly-
(iv) DUNNIGAN et al.87 studied
on CHD prevalence.
changes
sucrose intake comparable of long-term
“sucroseperipheral
than that
being 4 weeks. They concluded that glucose tolerance, were not significantly
with
hyperinsulinism
less, and serum cholesterol
ceride levels and their bearing the effects of iso-caloric
using students
developed
from a mean of 85 g to 12 g. On this regimen,
22%
in
(ii) YUDKIN
diets were 2 weeks.
who exhibited
decreases in lipid levels, however, synchronized emphasized
however,
sucrose intake,
the bearing of body weight on the magnitude during carbohydrate-rich
of sucrose
does a higher sucrose intake promote ischaemic
precludes
of sucrose.
Intakes
in patients
on the saw
5 times greater
this observation
effect,
fat indicated
of calories.
a third
on high- and low-sucrose
students,
a mean weight gain increment high sucrose regimen;
noted,
that
activity.
fat. 40%
intake
also reported
hyperlipidaemic
fat
had no effect on glucose toler-
They
on a high sucrose
on the
high in polyunsaturated
and low in cholesterol
exhibited
undertaken,
and fat in hyperlipoproteinaemic
whereas
ance test,
starch
or were not
will be mentioned.
(i) LITTLE relationship
have been
starch diets, than on low sucrose-high
in lipid levels,
in other studiesTs-87.
While, as noted,
investigations
In some of the trials undertaken,
found to be higher on high sucrose-low observed
and in smoking.
studies have been made, several short-term
their period of observation
plasma insulin and serum lipids
of sucrose for starch
at levels of
to those in western diets. These workers stressed the need
studies.
ADDITIONAL REQUIREMENTS OF EVIDENCE As indicated to the response
in the INTRODUCTION, a further
of experimental
.4thevosclerosis,1971, 14: 137-152
animals
key type of information
to sucrose.
An additional
relates
need concerns
SUGAR
INTAKE
information
AND
COROK;ARY
HEART
on the metabolic
serve to differentiate lipidaemia
mechanisms
between
on eq5erintedal
some workersgs-95
the converse
reported
cholesterolaemic studies, and
have been reported
in certain
and atherogenic the differences
Mechanisnz
of metabolic
his studies
dietary
than sucrose.
in responses
starch
was more hyper-
In the foregoing
and other experi-
and physical
m~ome
to high s~tc~ose itztakc. averred
opens up a new approach
disease, but with obesity,
inactivity,
that
diabetes,
agents into a single and plausible
“carefully
controlled
been consuming
is the validity
studies
hypothesis”.
Nevertheless,
considered
that “the hyperlipidemic
for the differences
the mechanism
that
CHD have
effect of sucrose may depend (2) the amounts of saturated in the diet”. It is probable
in the results
of the lipaemic probably
effect
studies
are mainly
with increments pathway
on rats,
cited,
with in ab-
from the circulation.
From
of rates
“the
of lipogenesis,
of enzymes of the hexose monophosphate
carbohydrate
the mechanism
compared
by differences
due to the stimulation
in the liver, coupled with relative
is needed to elucidate
of sucrose,
et aZ.90
ANTAR
et al.100 took the view that
MUKHERJEE
in the activities
of specific lipid classes on respective
obtained.
are regulated
and in the rate of removal of lipid components (on lipid levels)
hydrate
who develop
related to change in weight, and even to the sex and age of sub-
is not clear, but changes
their experimental
oxidative
a fundamental
of the belief (to which he still adheres)
fat, and (3) the amount of cholesterol
account
that
etc.,
smoking,
these possible
in these respects in the diets used in the various investigations
as well as problems largely
cigarette
of uniting
more sugar than those who do not”.
and polyunsaturated that differences
YUDKIN~~,
of ‘sucrose-
not only with CHD and peri-
hypertension,
on (1) the per cent of total calories as sucrose and starch,
associated
on the
to the problem of atherogenesis”.
have shown that individuals
t’t aZ.90 speculated
ANTAR
Recently,
“the discovery
may well provide a basis “capable
premise to his hypothesis
effects
firm conclusions
in respect of changes in both serum
His view is that the raised levels of insulin associated pheral vascular
sorption,
with
et a1.97,
E~RITCHEVSKY
contexts,
noted preclude
with starch diets,
just mentioned86991,
induced hyperinsulinism’
starch,
Using rats,
atherogenesis.
discussing
jectssg,
to influence
animals.
of lipid values on sucrose compared
has been found by other+.
that
role of high sucrose compared
etiologic
which could
of sucrose in hyper-
and other lipids in experimental
have noted elevations
regimens;
using rabbits,
lipids
involvement
Carbohydrates
animals.
the levels of serum cholesterol
mental
involved in man and animals,
a true or apparent
and atherogenesis.
Studies
starch
147
DISEASE
lowering of the catabolic
regimens”.
of the metabolic
Much further
response
to different
rate
research carbo-
foods.
COMMENT
The Medical
Research
countries was shown by YUDKIN
Councils4
report
stated
that
“sugar
intake
to be more closely related to mortality .-ltherosclwosis,
in various
from coronary 1971, 14: 137-152
A.
148 heart disease than any other nutrient”.
YUDKIN~~ used national
data from the same
sources as have been used in the present study. The first drawback disparity, intakes;
mentioned
earlier, between estimates
this considerably
demiological countries;
purposes.
limits
YUDKIN’S generalization
all were sophisticated
populations.
known to occur in some under-developed health
problem,
promote
demonstrates
that
depends in large measure
of a risk factor,
even innocuous
in anotherial~iaa.
The investigations heart
A very important
countries
(Table
point to emerge,
(with one exception)
investigations;
for example,
intake of the ischaemic this incongruity intake
or
yet far less so or
of YUDKIN et ul.z7Js, of the disease.
is that the mean daily intake study24, namely,
of the 146.6 g,
in the other
groups
of HOWELL AND WILSOK~~, the sugar
heart disease group was only 67 g pev dieln. On the one hand,
still further
in the development
lessens the role that can be accorded the validity
of the “control”
other than his own. The Medical Research
groups by the Medical
his findings, Research
groups
to know
(1) whether
and (2) whether
Council
Working
Party
that
in investigations
Council study24 was vehemently
It would be illuminating
YUDKIN could duplicate
to a high sugar
of CHD. On the other hand, it must be mentioned
YUDKIN~O~ has questioned in this respect.
or
with and without evidence
than that in the heavt disease
in the study
cause
or risk factor
of a nutrient,
in one context,
control gvoz~f~ (i.e. with no evidence of CHD) in the Scottish was far greater
nutrient
factor in the development
moreover,
no major
PeY SE does not
2), apart from the studies
sugar as a significant
of sugar
where CHD presents
prevailin g; a high intake
may be deleterious
for epiin fifteen
the very high intakes
on the sugar intake of populations
disease
failed to incriminate
Yet
and of household
information
to populations
effects of a particular
on the context
high prevalence
related
in such data is the
intakes
intake
a high sugar intake
CHD. Clearly, the deleterious
of ischaemic
of national
the value of national
R. P. WALKER
criticized
in further
studies
the use of correct
control
would significantly
alter
their final conclusion. In diseases of d@cielzcy -
specific incrimination
YUDKIX~O~) is relatively with excess of nutrients
kwashiorkor,
of particular simple.
rickets, scurvy, iron deficiency anaemia,
nutrients
In a number
(using the criteria
that
major
such as fluorosis, also siderosis from iron overload,
apportion-
But the situation
role to a single nutrient
is feasible,
on the global interracial
research
Atherosclerosis,
14:
137-152
the issue, and
such as sugar,
as the cause
In so far as ascribing a promotive
on such a problem
should not be con-
groups within western populations
less CHD than their national
1971,
complicate
aspects where the variables are numerous. Attention
should rather be focussed on minority significantly
is far less straightforward
It cannot therefore be expected
of a single food component,
of CHD will emerge from current or future research. centrated
factors
and possibly racial factors operate.
incrimination
by
associated
with diseases such as CHD, where other nutritional where non-dietary
put forward
or diseases
ment of blame again presents no difficulty.
of conditions
average.
who have
SUGAR
IXTAKE
AND
COROS_%RY
HEART
119
DISEASE
REFERENCES CAMPBELL, M., The mortality rate from heart disease (Editorial), -4ww. Heart J., 1964, 68: 1, ROBB-SMITH, A. H. T., The E~zigma of Coromz~~~ Heart Disease, Lloyd-Luke, London, 1967, p. 109. CLEAVE. T. L., G. D. CAMPBELL .U?D S. S. PAINTER, Dznbetes, Coromrv Thrombosis, artd the Saccharine Disease, 2nd edition, Wright, Bristol, 1969, p. 124. KEYS, .A., The diet and atherosclerosis. In : M. SANDLER AND G. H. BOURNE, (Eds.), .-lthevosclerosis and its Uvigirz, i\cademic Press, New York, 1963, pp. 263%299. STAMLER, J,, Nutrition, metabolism, and atherosclerosis. 4 review of data and theories, and a discussion of contra\-ersial questions. In: F. J, INGELFINGER, A4. S. REL~IAN AND 31. FINLAND (Eds.), Controwrs_v ix Irzterml :Wedicimz, Saunders, London, 1966, pp. 25559. NATIONAL DIET-HEART STUDY. Circulation, 1968, 37: Suppl. No. 1. FRIEDI\IAN,M., Pathogeuesis of Covonav?, .1rteyy Dzsense, McGraw-Hill, New T;ork, 1969, p. 75. HICRIE, J. B., The preVention of coronary heart disease, ,lfed. J. .-lzsstrol.,1968, i: 159. MALXROS, H., Dietary prevention of atherosclerosis, Lnncet, 19fi9, ii: 910. MASIROYI, R., Dietary factors and coronary heart disease, R&l. TY.H.O., 1970, 42: 103. LEREN, P., The Oslo Diet-Heart Study: Eleven year report. Circulatioz, 1970, 42: 935. Current Aspects of Cardiology, Bat. Med. J., 1969, 3: 16. WALKER, A. R. P., Coronary heart disease - are there differences in racial susceptibility? .dmer. J. Epidemiol., 1969, 90: 359. Rome, 1969, 7968, Food and Agriculture Organisation, The State ofFood aud .Igvicultwe, p. 168. WORLD HEALTH ORGANISATION,.-lvtevioscZerotic a)ld Degeuevatiw Heart Disease (\Vorld Health Statistics Report, No. 22), 1969, p. 462. YUDKIN, J., Diet and coronary thrombosis: Hypothesis and fact, Lnrzcet, 1957, ii: 155. OSANCOVA. I<., S. HEJD.~ AND Ii. ZVOLANKOVA, Dietary fat and dietary sugar, Lmcet, 1965, i: 494. ASHTON, 1%:. L., Dietary fat and dietary sugar, Lnnret, 1965, i: 653. STOCKS, I’., Heart disease mortality in cities of Latin America and in cities and regions of England and Wales, Bull. TI’.H.O., 1969, 40: 409. Domestic Food Coxsumptioui md Expenditure, 7967 (Annual Report of the National Food Sur\Tey Committee), H. M. S. 0.. London, 1963, p. 13. KEYS, A., Coronary heart discase in seven countries, (Editorial), Circ~laliorz, 1970, 41: Supplement No 1. WALKER, A. R. P., Problems in studying the epidemiology of coronary heart disease in unsophisticated populations (Editorial), .4+xer. Heart J., 1970, 80: 725. YUDKIN, J,, Measurement of sugar consumption by questionary, Bit. Med. J., 1967, 3: 154. WORKINCI PARTY, MEDICAL RESEARCH COUNCIL, Dietary sugar intake in men with m)-ocardial infarction. Lancet. 1970. ii: 1265. Hypertensim and Coronar~~ Heart Studies (Worid Health Organization
Disease:
Technical
Classijicatiox
and
Critevia
forEpidemiological
Report Series, No. 163), World Health Organi-
zation, Genela, 1959, p. 14. ROSE. G. A. AKD H. BLACKB~RN, Cnrdioruzscular Szcvvev Methods (World Health Organisation. Monokraph Series, ?;o. 56), \Vorld Health Organization, Geneva‘, 1968, Ch. 4. YUDKIN, J. AND J, RODDY, Levels of dietary sncrosc in patients with occlusive atherosclerotic disease, Lancet, 1964, ii: 6. YUDKIN, J. AND J. MORLAND, Sugar intake and myocardial infarction, Amer. J. Clip. X&v., 1967, 20: 503. LITTLE. 1. 11.. H. M. SHSNOFF, .4. CSIMA, S. E. RED~XONDAND R. YANO, Diet and serum-lipids in malt survivors of myocardial infarction, Lmcet, 1965, i: 933. PAPP. 0. A.. L. P~DILLA AND A. L. TOHNSON,Dietarv intake in patients with and without myocardial infarction, Lmcet, 1965, ii: 259. PAUL, O., A. MACMILLAN, H. MCLEAN AND H. PARK, Sucrose intake and coronary heart disease, Lancet, 1968, ii: 1049. FINIXAN, A., K. HICKEY, B. MAURER AND R. MULCAHY, Diet and coronary heart disease; dietary analysis on 100 male patients, Amer. J. Clin. A’utr., 1968, 21: 143. _ FINEGAN, A.. N. HICKEY, B. MAURER AHD R. M~LCAHY, Diet and coronary heart disease: dietary analysis on fifty females, .4nzer. J. Clsn. Nuts., 1969, 22: 8. HOWELL, R. W. AND D. G. WILSON, Dietary sugar and ischaemic heart disease, Bril. Jled. .I., 1969, 3: 145. BURNS-C• X, C. J., R. DOLL AND Ii. P. BALL, Sugar intake and myocardial infarction, Bvit. Heart J., 1969, 31: 485. BENNETT, A. E., R. DOLL AND R. W. HOWELL, Sugar consumption and cigarette smoking, Lmcet, 1970, i: 1011. _ltherosclevosis.
1971, 14: 137-152
150
A. R. P. WAL.UER
ELWOOD, P. C., W. E. WATERS, S. MOORE AND P. SwEETxAnI, Sucrose consumption and ischaemic heart disease in the community, Lamet, 1970, i: 1014. KEEN, H. AND G. ROSE, Dietary fat and dietary sugar, Lancet. 1964, ii: 362. BEGG, T. B., S. R. PRESTON AND M. J. R. HEALY, Atti de1 \’ Convegno Internazionale sugli Aspetti Dietetici dell’ Infanzia e della Senescenza, Rome, 1966, p, 66. YUDKIN, J., Dietary prevention of atherosclerosis, Lancet, 1969, 2: 1072. GUGGENHEIM,Ii., Y. WEISS AND M. FOSTICK, Composition and nutritive value of diets consumed by strict vegetarians, Brit. J. Nub., 1962, 16: 467. MARR, J. W. AND J. A. HEADY, Levels of dietary sucrose in patients with occlusive atherosclerotic disease, Lancet, 1964, ii: 146. EPSTEIN, F. H., R. SIMPSON AND E. P. Boas, Relations between diet and atherosclerosis among a working population of different ethnic origins, Amer. J. Clin. A\rutr., 1956, 4: 10. WALKER, A. R. P., Extremes of coronary heart disease mortality in ethnic groups in Johannesburg, South Africa (Editorial), .41vzer. Heavt J., 1963, 66: 293. WALKER, A. R. P., C. M. HOLDSWORTHAND E. J.WALKER, Investigationsonthe consumption of sugar by South African populations, S. _4jr, jled. I,, 1971, 45: 516. WALKER, A. R. I’., Mortality from coronary heart disease and from cerebral vascular disease in the different racial populations in South hfrica, S. rlfr. died. J., 1963, 37: 1155. WYNDER, E. L., F. R. LESSONAND I. J. BROSS, Cancer and coronary artery disease among Seventh-Day Adventists, Caxceu, 1959, 12: 1016. HARDII\TGE, M. G. AND F. J. STARE, Nutritional studies of vegetarians, Part 1 (Nutritional, physical, and laboratory studies), rll?zer. J. Clirz. Sutv., 1954, 2: 73. ELLIS, F. R. AND V. M. E. MONTEGRIFFO, Veganism, clinical findings and investigations, .~++zPY. J. Clitz. Nutr., 1970, 23: 249. JERVELL, A., I<. MEYER AKD I<. \VESTLUND,Coronary heart disease and serum cholesterol in males in different parts of Norway, dcta ;lIed. Stand., 1965, 177: 13. BERKSON, D. hl., J. STAMLER, H. A. LINDBERG, IV. MILLER, H. MATHIES, H. L-\SKY AND Y. HALL, Socio-economic correlates of atherosclerotic and hypertensive heart diseases, A432~. N.1’. .4cad. Ski., 1960, 84: 835. Food Consurxption ofHouseholds ix the Novth East, Spring, 1965. U.S. Dept. Agric. Household Food Consumption Survey, 1965-66, Report No. 2, July, 1968. Food Comzrmptio~t ofHouseholds in the South, Spring, 7965. U.S. Dept. rlgric. Household Food Consumption Survey, 1965566, Report No. 4, July, 1968. SAUER, H. I., Epidemiology of cardiovascular mortality - geographic and ethnic, .4nzer. J. Pub. Health, 1962, 52: 91. SEFTEL, H. C., M. C. KEW AND I. BERSOHN, Myocardial infarction in Johannesburg Bantu, S. .4fr. ;2Ied. J., 1970, 44: 8. SARVOTHAM, S. G. AND J. N. BERRY, Prevalence of coronary heart disease in an urban population in northern India, Civrzllation, 1968, 37: 939. EPSTEIN, F. H., L. D. OSTRANDER, B. C. JOHNSON,M. TV. PAYNE, N. S. HAYNER AND J. B. KELLER, Epidemiological studies of cardiovascular disease in a total community - Tecumsch, Michigan, .412n. Intern. ,Wed., 1965, 62: 1170. WYSH~M, D. N., Ii. C. I~OHLI AND S. MULHOLLAND,Coronary risk factors in Northern India, Amev. Heart J., 1970, 79: 181. EDITORIAL, Brown bread ZXYSZIS white, Brit. Med. J., 1937, 2: 752. SMITH, E., Dietaries in the workhouses of England and \Vales, Brit. Med. J., 1871, 2: 222. ORR, J. B., Food Health and Izcome, Macmillan, London, 1936, p. 17. DRUMMOND, J. C. AND A. WILBRAHAM, The Englishman’s Food, Jonathan Cape, London, 1939, p. 388. ODDY. D. T.. Food in nineteenth-centurv _ England: Nutrition in the first urban societv.i v Proc. k~tr.*&, 1970, 29: 150. WALKER, A. R. P., Crude fibre, bowel motility, and pattern of diet, S. .4fr. Xed. J., 1961, 35: 114. ~URKITT, D. P., Relationship as a clue to causation, Laxcet, 1970, ii: 1237. SPRAGUE, H. B., The search for the “coronary” archetype and the Damocles Test (Editorial), Circulation, 1966, 33: 676. HATCH, F. T., P. K. REISSELL, T. M. W. POON-KING, G. P. CANELLOS, R. S. LEES AND L. M. HAGOPIAN, A study of coronary heart disease in young men, Circulation, 1966, 33: 679. WALKER, A. R. P., The prevention of coronary heart disease (Editorial), dmer. Heart J., 1966, 72: 721. PAGE, I. H. AND H. B. BROWN, Some observations on the National Diet-Heart Study (Editorial), Circulation, 1968, 37: 313. MACDONALD, I. AND D. M. BRAITHWAITE, The influence of dietary carbohydrates on the lipid pattern in serum and in adipose tissue, Clin. Sci., 1964, 27: 23.
4therosclerosis,
1971, 14: 137-152
SCGAR
INTAKE
AND
COROSARY
HEART
151
DISE.4SE
M. A. AND M. A. OHLSON, Effect of simple and complex carbohydrates upon total lipids, non-phospholipids and different fractions of phospholipids of serum in young men and women, /. A’utr., 1965, 85: 329. 73 KAUFMANN, N. A., R. POZNANSKI, S. H. BLONDHEI~I AND Y. STEIN, Changes in serum lipid levels of hyperlipemic patients following the feeding of starch, sucrose, and glucose. .4mev. J. Cl&. iv&r., 1966, 18: 261. 73 MCGANDY, R. B., D. M. HEGSTED, M. L. MYERS AND F. J. STARE, Dietary carbohydrate and serum cholesterol levels in man, .-l SPY. J. Cli~z. N&Y., 1966, 18: 237. 74 COHEN, A. M., A. TEITELBAUM, M. B~LOGH AND J. J. GROEN, Effect of interchanging bread and sucrose as main source of carbohydrate in a low fat diet on the glucose tolerance curve of healthy volunteer subjects, .-1mer. J. CZin. N&r., 1966, 19: 59. 75 Kuo, P. T., L. FENG, N. N. COHEN, IV. T. FITTS AND L. D. MILLER, Dietarv carbohrdrates in hyperlipemia (hyperglyceridemia) ; hepatic and adipose tissue lipogcnic activities,‘.-1 nle~. J, Clirz. .vz~tr., 1967, 20: 116. 76 NESTEL, P. J,, Ii. F. CARROLL AND N. H.-\VENSTEIN, Plasma triglyceride response to carbo1970, 19: 1. hydrates, fats and caloric intake, Aletab. Cliu. Exp., 77 K\NN, J. I., A. S. TRUS~ELL, D. A. HENDRICKS AND F. hl_4xxIPic, Effects on serum-lipids in normal men of reducing dietary sncrosc or starch for five months, 1_.aixet, 1970, i: 870. 7s .%NDERSON, J. T., F. GR.INDE, Y. M~TSU?IOTO AKD A. KEYS, Glucose, sucrose and lactose in the diet and blood lipids in man, J, Sxlv., 1963, 79: 349. 7Q LEES, R. S., The plasma response to two t\-pcs of dietary carbohvdratcs, Cli~z. Res., 1965, 13: 549. 8” GRANDE, I;., J. T. ANDERSON .~ND A. KEYS, Effect of carbohydrates of leguminous seeds, wheat and potatoes on serum cholesterol concentration in man, J. 9z~tv., 1965, 86: 313. *I PORTE, JR., D.. E. L. BIERR~.~N AND J, D. B.~GDADE, Substitution of dietary starch for dextrose in hyperlipemic subjects, Pmr. SM. E.rp. BfoZ. .Ued., 1966, 123: 814. 8s nfCGr\NDY, R. B., D. M. HEGSTED AND 1;. J. ST.IRE, Dietarv fats, carbohydrates and atherosclerotic vascular disease, Sezc~ EilgZ. J. _Iled., 1967, 277: 166 and 242. 83 DALDER~P, L. M., R. DOORNBOS ;\ND J. E. DE \-RIES. Dietary sugar and serum-cholesterol, Lnxet, 1968, 1: 819. 84 ANTONIS, .\., C. ILES .?ND T. Ii. E. PILKINGTON, The effects of dietary carbohydrate on serum lipid levels, Pvoc. X&r. Sot., 1968, 27: 2A. 85 DOLDERUP, L. M., R. DOORNBOS, C. DEN HORTON, W. B. Sari H.4.4RD, J. E. DE VRIES .4xo G. H. 11. KELLER, A practical method for decreasing the serum cholesterol level in man, .-fnzev. J. CZilz. N&r., 1969, 22: 1521. The effect of dietary sucrose on blood lipids, serum insulin. % Sz.4~~0, S. .~ND J. YUDKIN, platelet adhesiveness and body weight in human volunteers. Pos!gvad. Med. J., 1969, 45: 602. 87 IIUNNIGAN, hf. G., T. FYFE, M. T. McIiIDDIE AND S. M. CROSBIE, The effects of isocaloric exchange of dietary starch and sucrose on glucose tolerance, plasma insulin and serum lipids in man, Cli~z. Sci., 1970, 38: 1. ** LITTLE, J. A., B. L. BIRCHWOOD, D. .\. SIMMOXS, M. A. L1~~r.\~, I\. K~LLOS, G. C. BUCKLEY END .A. CSIM~, Interrelationship between the kinds of dietary carbohydrate and fat in hyperlipoproteinemic patients, Part 1 (Sucrose and starch with polyunsaturated fat), .4thevoscZerosis. 1970,ll: 173. *Q BIRCHWOOD, B. L., J. A. LITTLE, M. ‘2. L\NTSR, C. LUCAS, G. C. BUCKLEY, A. c‘s1x.4 ANI) _a. KALLOS, Interrelationship between the kinds of dietary carbohydrate and fat in hyperlipoproteinemic patients, Part 2 (Sucrose and starch with mixed saturated and polyunsaturated fats), _lfhevoscZerosis, 1970, 11: 183. 90 ANTAR, M. ;I., J. A. LITTLE, C. Lucas, G. C. BUCKLEY AND A. Cs1nl.4, Interrelationship between the kinds of dietary carbohydrate and fat in hypcrlipoproteinemic patients, Part 3 (Synergistic effect of sucrose and animal fat on serum lipids), Atherosclerosis, 1970, 11: 191. 91 YUDKIN, J., S. SZANTO AND V. V. K.~KK~R, Sugar intake, serum insulin and platelet adhesiveness in men with and without peripheral vascular disease, Posfgvad. -Wed. J., 1969, 45: 608. intolerance and lipemia, A $L)&.Ixter,~. 92 BIERMAN, E. L. AND D. PORTE, JR., Carbohydrate Med., 1968, 68: 926. 93 STAUB, R. \V, AND R. THIESSEN, JR., Dietary carbohydrate and serum cholcstcrol in rats. Fed. Proc., 1967, 26: 490. 94 I'ORTMAN, 0. W., E. Y. LAWRY AND D. BRUNO, Effect of dietary carbohydrate on experimentally induced hypercholesterolemia and hyperbetalipoproteinemia in rats, Pvoc. Sot. Exp. Biol. Med., 1956, 91: 321. 95 VIJ~YAGOP~LAN, P. AND P. A. I(URUP, Effect Of dietary starches on the serum. aorta and hepatic lipid levels in cholesterol-fed rats, ‘4 themsclerosis, 1970, 11: 257. 96 ANDERSON, T. A., Effect of carbohvdrate source on serum and hepatic cholesterol levels in the cholesterol-fed rat, Proc. Sot. Exp. Biol. Med., 1969, 130: 854. 71 ANTBR,
~~therosrlerosis,
1971, 14: 137-152
A. R. P. WALKER
152
97 KRITCHEVSKY, D., P. SaLL.4T.4 AND S. h. TEPPER, Experimental atherosclerosis in rabbits fed cholesterol free diets, J. Atheroscler. lies., 1968, 8: 697. 98 YUDKIN, J., Sucrose, insulin, and coronary heart disease, Avnev. Heart J,, 1970, 80: 844. 9s KAUFM~NN, N. A. AND Y. STEIN, Carbohydrate induced lipemia (Editorial), .itheroscZerosis, 1970, 11: 365. 100 MUKHERJEE, S., M. Basu AXD Ii. TRIVEDI, Effect of low dietary levels of glucose, fructose and sucrose on rat lipid metabolism, Atherosclerosis,1969, 10: 261. 101 LO~~ENSTEIN, F. W., Epidemiologic investigations in relation to diet in groups who show little atherosclerosis and are almost free of coronary ischcmic heart disease, Amer. J. Cliw. N&r., 1961, 15: 175. 102 WALKER, A. R. P., Interpretation of biological data on one ethnic or regional group may not be equally applicable to other groups, A~rzer. J. Clix. Nutr., 1967, 20: 1025. 103 YUDKIN, J., Sugar consumption and myocardial infarction, Lancet, 1971, i: 296. 104 YUDKIN, J., Fatty acids and coronary disease, Practitiorw, 1961, 187: 150.
4therosclerosis,
1971, 14: 137-152