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Influence of Nutritional Factors on

Prevalence of Diabetes
Kelly M. West, M.D., and John M. Kalbfleisch, M.D., Oklahoma City

some of the same methods were used in testing two


SUMMARY communities in the United States.1'3 The epidemiologic
Twelve age-matched populations of eleven countries were studies previously reported in these twelve populations
tested by standardized methods to determine associations of three continents included observations on preval-
between prevalence of hyperglycemia and certain epidemio-
ence of hyperglycemia in relation to several factors in-
logic variables, including several nutritional factors. There
were great differences among some of these populations in cluding age, sex, parity, birth weights of children, race,
socioeconomic status, diet, adiposity, and race. Environ- and socioeconomic and rural-urban status.1-2 Nutri-
mental and demographic circumstances varied widely and tional data were also reported. In this paper, additional
prevalence of diabetes differed as much as ten-fold. There information will be given concerning the diet in six of
was in general a positive association between prevalence of
diabetes and dietary intake of fat and of sugar, and a the countries; and the prevalence of hyperglycemia in
negative association between prevalence of diabetes and the various populations will be related to serum choles-
total carbohydrate consumption; but some inconsistencies terol levels, electrocardiographic status, and the dietary
in these~Threc"as5ociaii6ns suggested that they may have intake of carbohydrate, protein, fat, and sugar. Popula-
been partly or completely coincidental. Prevalence of dia- tions were tested in Uruguay, Venezuela, Malaya (now
betes correlated well with serum cholesterol levels, both
among and within populations. Thejnost impressive and Malaysia), East Pakistan, Costa Rica, El Salvador, Gua-
consistent association in these studies was between pre- temala, Honduras, Nicaragua, and Panama.
valence of "diabetes and fatness (as estimated by weight Although an association between adiposity and preva-
in relation to lieTghT)7 Both within and among countries lence of diabetes has been observed repeatedly, the ex-
and races, this association was observed to a high degree.
Interracial differences in prevalence of diabetes were small tent to which, and the circumstances under which,
when racial groups were matched for adiposity. nutritional factors influence prevalence of diabetes have
In a group of 1,645 subjects from the general population not been determined precisely. Indeed, O'Sullivan et
of Central America, those with abnormal glucose tolerance al. followed for seventeen years a group of obese peo-
had a substantially higher prevalence of electrocardio- ple whose blood glucose levels were initially normal,,
graphic abnormalities than those with normal tolerance. and found no significant increase in the incidence of
DIABETES 20:99-108, February, 1971.
diabetes as compared to the nonobese in the same popu-
lation.4 Moreover, the hypothesis that diabetes causes
obesity is still under consideration.5 It has also been
The purpose of this report is to present further
suggested that specific dietary components such as
data on the relationships between the prevalence of
sugar6 and fat7 may increase susceptibility to diabetes.
diabetes and certain epidemiologic variables, particu-
Among the problems which have made it difficult to
larly nutritional factors. Results of studies in four of
evaluate the associations between prevalence of diabetes
the countries were published in 1966.1 More recently,
and nutritional factors have been the paucity of syste-
it has been possible to compare the former results with
matically collected data on nutrition in populations
data from six additional countries.2 It has not been
where prevalence of diabetes has been established (and
possible to compare directly the results in these ten
vice versa), the lack of uniformity in methods and
countries of Asia, South America, and Central America
definitions, and difficulties in obtaining representative
with the general population of the United States, but
samples of age-matched populations. Our methods did
not overcome all of these difficulties, and in several
From the Department of Medicine, University of Oklahoma respects our data are less than ideal; but we were able
School of Medicine, Oklahoma City, Oklahoma.

FEBRUARY, 1 9 7 1 9S>
INFLUENCE OF NUTRITIONAL FACTORS ON PREVALENCE OF DIABETES

to test ten population samples which were at least precise measure of body adiposity, but in general it is
crudely representative, and use of standard procedures well correlated with fatness.8-15 We therefore deter-
and criteria permitted some comparisons which were mined the weight of each subject in relation to a stand-
not possible heretofore. ard for his height in order to calculate a per cent of
standard weight.8 This standard is age-independent. It is
METHODS based on data published by the Society of Actuaries in
In ten countries, the diabetes-related studies were 1959 for a group of Americans from twenty to twenty-
part of detailed nutrition surveys. The methods em- nine years of age.8 Although this arbitrary standard was
ployed have beeen described in detail.1'2-8'14 The stud- adopted by the Interdepartmental Committee on Nutri-
ies in the six Central American countries included the tion as a means for expressing weight in relation to
selection and testing of representative population sam- height, it was not assumed that 100 per cent of stand-
ples, clinical examinations, extensive biochemical de- ard necessarily represented ideal weight either for young
terminations in representative subgroups, dietary cal- or older aduits.
culations based on interviews with representative fami- The results reported here are confined to the seg-
lies using standard methods, and food measurements ments of the population over thirty years of age. In
and analyses. most countries, only subjects over thirty-four years of
Similar studies had been conducted previously in age were included in the diabetes-related studies, but
Uruguay, Malaya, East Pakistan, and Venezuela.1 How- the nutrition studies included all ages. Details con-
ever, in the latter four countries, methods of popula- cerning the frequency distributions of ages for each of
tion sampling were less systematic and refined. For ex- these populations have been published.1-2 The fre-
ample, in Venezuela, a total of 480 subjects from the quency distribution of the ages was very similar for
general population were tested for diabetes in fifteen each of these populations; the mean age varied only
arbitrarily selected sites in six different regions of the from forty-eight years in East Pakistan to fifty-two
country. Although an attempt was made to test repre- years in Venezuela. In contrast to the other methods,
sentative subjects of representative communities, the which were standardized, the method for measuring
unsystematic methods used and other sources of poten- plasma cholesterol varied among the countries. Cho-
tial bias were such that this could not be considered a lesterol determinations were not performed in the same
truly representative national sample of the kind ob- laboratories, but all values for the six countries of Cen-
tained in the Central American countries. tral America were measured in the same laboratory by
The number of testing sites ranged from thirteen in the AutoAnalyzer technic based on modifications of the
Uruguay to forty in Guatemala. In Uruguay, 484 sub- Zak method.16 In Venezuela and East Pakistan, the
jects were tested for diabetes; in East Pakistan, 513 method used was that described by Searcy, Bergquist,
were tested; and in Malaya, 566 participated. Details and Jung.17 In Uruguay and Malaya, the method used
published previously concerning the Central American was that of Carpenter, Gotsis, and Hegsted.18 Details
studies include population characteristics, methods, sam- have been reported previously concerning the glucose
pling procedures, and the numbers tested in the various tolerance tests.1-2 Each subject received one gram of
countries.2 glucose per kilogram of body weight. Subjects whose
Diets varied somewhat from region to region within two-hour venous blood glucose levels exceeded 149
countries, and there were of course differences among mg./ioo ml. were classified as diabetic, but because
individuals in the quality and quantity of diet. The frequency distribution data have been published, rates
average figures given below for each population repre- of "diabetes" can be calculated for all countries using
sent only the mean consumption per capita, but, in diagnostic standards that are either higher or lower than
general, the qualitative interindividual variations in the arbitrary criterion we employed.
diet were small. Figures are not presented here for Twelve-lead electrocardiograms were performed. In-
caloric intake because of the complexity of these cal- terpretation of the electrocardiographic data is compli-
culations and the lack of precision of these methods,8 cated in some respects by the fact that in every coun-
but these data have been reported.1'9"14 Under the field try electrocardiography was with rare exceptions per-
conditions which prevailed, the best available index of formed thirty to 180 minutes after glucose loading.
caloric intake (in relation to energy expenditure) was Because glucose loading sometimes produces certain
weight in relation to height. This is not of course a kinds of electrocardiographic changes,19"24 the implica-

DIABETES, VOL. 2O, NO. 2


KELLY M. WEST, M.D., AND J O H N M. KALBFLEISCH, M.D.

TABLE 1
Relationship in Central America between adiposity and prevalence of abnormal or borderline glucose tolerance

Weight as per cent of standard Two-hour blood glucose


>149 mg,/100 ml. 120 to 149 mg./lOO ml.
Mean
Age
<80% 57 3% 5%
Very lean 80-89% 53 3% 7%
Lean 90-99% 50 3% 6%
Medium 100-109% 50 3% 6%
Thick >109% 50 10% 12%

tions of this phenomenon are reviewed in the Discus- sylvania1 as in Central America, but rates of diabetes
sion. were not significantly different when the two popula-
RESULTS tions were matched for adiposity.
Figure 1 shows the marked contrast in the fatness
Relationship between adiposity and prevalence of
(per cent of standard weight) of the populations of
diabetes: In studying the relationship between preval-
ence of diabetes and many factors in the different coun- East Pakistan, Uruguay, and Central America (data for
tries, the most impressive correlation has been with fat- all six countries lumped). The rates of "diabetes" for
ness.1*2 Table i shows the relationship of adiposity age-matched segments of these populations (East Pak-
(per cent of standard weight) and prevalence of "dia- istan, 2.5 per cent, Central America 4.1 per cent, and
betes" in the Central American subjects (data for all Uruguay, 6.9 per cent) reflect closely these differences
countries lumped). Impairment of glucose tolerance was in fatness. While the correlation between overnutri-
more than three times as common in the subjects whose tion and prevalence of diabetes has been quite consis-
weights exceeded 109 per cent of standard as in the tent in the groups we have studied, a protective effect
remainder of the population. of undernutrition (marked leanness) has been observed
Table 2 shows the frequency distribution of per cent less consistently. In Asia, diabetes was definitely more
of standard weight by sex for the Central Americans, common in those whose weights were "normal" (90-
all of whom were over thirty-four years of age. The 109 per cent of standard) than in very lean persons
mean per cent of standard weight for males was 95 per (weight less than 90 per cent of standard). The rate of
cent. The mean adiposity of the females was signifi- diabetes in the very lean subjects was 1.7 per cent, while
cantly greater, 103 per cent of standard. We analyzed the rate for those of normal weight was 4.9 per cent
data from the U.S. National Health Survey25 with re- [difference statistically significant (p < . o i ) ] . But in
spect to mean per cent of standard weight for ages the eight countries of Latin America, diabetes was only
matching those of our Central American subjects. The slightly less common in the very lean subjects than in
mean per cent of standard weight of U.S. males was those with normal weights, and the difference was not
i n per cent and for females 113 per cent. Diabetes statistically significant. In all these countries, however,
was about four times as common in Bangor, Penn- the mean age of the very lean subjects was greater than

TABLE 2
Frequency distribution of per cents of standard weight in Central America by sex

Frequency distribution (by per cent) of weight


(expressed as per cent of standard weight)
Per cent of standard weight <70 70 to 79 80 to 89 90 to 99 100 to 109 110 to 119 120 to 129 >129 Total
Males 1.2 10.8 32.0 26.1 16.6 7.5 3.7 2.2 100.1
Females 1.8 8.4 20.5 21.8 16.5 11.9 7.9 11.3 100.1
Total 1.5 9.4 24.9 23.5 16.5 10.2 6.3 7.7 100.0
Total (Corrected*) 1.5 9.6 26.3 24.0 16.6 9.7 5.7 6.8 100.2
* Based on anticipated results if an equal number of males and females were tested. The observed results were influenced
slightly by the fact that more females than males were tested.

FEBRUARY, 1 9 7 1
INFLUENCE OF NUTRITIONAL FACTORS ON PREVALENCE OF DIABETES

• - • EAST PAKISTAN
40-
O - - O CENTRAL AMERICA
—A URUGUAY

a.
Z)
O
O

90 100 110 120 130


% STANDARD WEIGHT (MEAN)

FIG. 2. Association of diabetes prevalence and mean per cent


of standard weight. EP stands for East Pakistan, M
for Malaya, E for El Salvador, P for Panama, G for
Guatemala, H for Honduras, N for Nicaragua, C for
Costa Rica, V for Venezuela, and U for Uruguay.
Data for diabetes prevalence apply only to older
<70 70-79 90-99 110-119 > 129 segments of these populations (over thirty-four years}.

% OF STANDARD WT.
FIG. I. Frequency distribution of per cents of standard weights lations.1-2 Although older subjects had poorer glucose
for three populations. tolerance in all countries, associations between preval-
ence of diabetes and adiposity were not attributable to
the mean age of those of average weight (see below). a greater adiposity of older subjects. Comparable data
Although rates of diabetes differed markedly in Uru- concerning-the relationship between age and weight
guay, East Pakistan, and Central America, rates were were available for eight countries (Venezuela, East
not significantly different for these three populations Pakistan, and the six Central American nations). In
when matched for per cent of standard weight. In Cen- our subjects over thirty-four years of age, there was no
tral America the relatively high rates of diabetes in fe- increase in weight (expressed as per cent of standard
males, and for both sexes in Nicaragua and Costa weight) with age in any country. In most countries,
Rica,2 were entirely "corrected" when adjustments were weight increased between age twenty and age thirty-
made for the greater fatness of these three subgroups ica between "sociocultural status"9"14 and cholesterol
of the general population. There were some differ- before declining in old age. In all of the eight coun-
ences among groups and subgroups that were not en- tries, a significant decline in weight was observed be-
tirely corrected by matching for adiposity, but these ginning between age fifty-five and sixty-five. In each of
differences associated with other factors (such as race, the Central American countries, the relationship be-
sex, etc.) were modest.1'2 In all of these countries, tween age and weight was quite similar; when data
some of the diabetics had lost significant amounts of were lumped for all of our subjects in six countries,
weight because of diabetes. Thus, the association be- it was found that weight was 100 per cent of standard
tween adiposity and risk of diabetes is even stronger for subjects from thirty-five to forty-four years of age,
than suggested by these data. 100 per cent for those from forty-five to fifty-four years,
Figure 2 shows for ten populations the relationship 98 per cent for those from fifty-five to sixty-four years,
between diabetes prevalence and per cent of standard and 94 per cent for those over sixty-four years of age.
weight. The correlation coefficient for this association is Table 1 shows the mean age for each of five subgroups
very impressive (r of 0.89). in Central America with different degrees of adiposity.
Data have been reported previously on the relation- Diet: Table 3 summarizes the diets in each of eleven
ships between age and glucose tolerance in these popu- populations. The twelfth age-matched population tested

DIABETES, VOL. 2O, NO. 2


KELLY M. WEST, M.D., AND J O H N M. KALBFLEISCH, M.D.

TABLE 3 and other characteristics of the diet, including levels of


Diets and prevalence of diabetes* in eleven populations fat, animal fat, and protein. There was also a negative
association between total carbohydrate consumption
Diabetes Per cent of calories
prevalence Carbo- and the prevalence of diabetes, as shown in table 3. For
(per cent)* hydrate Sugar Protein Fat reasons described in the Discussion, these associations
East Pakistan 2.0 83 2 10 7
were not thought to have a cause and effect relation-
Malaya 3.3 68 8 11 21
Costa Rica 5.4 69 17 11 21 ship.
El Salvador 3.2 70 7 12 17
Guatemala 4.2 73 10 12 15 Cholesterol: Levels of dietary cholesterol in the vari-
Honduras 4.1 66 8 13 22 ous populations of Central America are not yet avail-
Nicaragua 5.0 66 12 13 21
Panama 2.5 67 9 11 22 able to us, but cholesterol intake is probably much
Uruguay 6.9 53 12 14 33
7.0 62 7 14 24
lower than in the United States because fat intake is
Venezuela
Bangor, Pa.f 17.2 47 13 40 substantially less than in North America, as shown in
* Venous blood glucose >149 mg./lOO ml. in subjects table 3. Also, the portion of fat which is of animal
over thirty years of age. These prevalence rates differ slightly origin (roughly half) is lower in Central America than
from observed rates because they have been adjusted to the
predicted rate if an equal number of males and females had in the United States.9"14 Plasma cholesterol levels for
been tested. 2,034 subjects (803 males and 1,231 females) in Cen-
t Crude estimates.1
Some totals do not add to 100 per cent because of tral America and the relationship of these levels to age
rounding.
are shown in table 4. Cholesterol levels did not rise
with age in either sex. On the contrary, in old age
for diabetes by these methods was the Cherokee Indians there was some decline in these values. This does not
of North Carolina, in whom the prevalence of dia- necessarily mean, of course, that old age was associated
betes was approximately 25 per cent.3 The diet of these with a decline in the cholesterol levels of individual
Indians was high in calories but qualitative dietary subjects. This phenomenon could be attributable in part
studies were not adequate to warrant presentation in or entirely to a higher rate of survival of those with
table 3. Table 3 also shows the relationship between low cholesterol levels, or to other factors.
several dietary factors and the prevalence of diabetes The relationship between glucose tolerance and
in these age-matched populations. In the twelve age- cholesterol level is shown in table 5. Cholesterol levels
matched populations we have tested, the prevalence of were substantially greater in those with impairment of
impaired glucose tolerance ranged from 2 per cent in glucose tolerance. In males, a statistically significant in-
the very lean Pakistanis to 25 per cent in the very crease in cholesterol values was observed even in those
fat Cherokees. with minimal impairment of tolerances (two-hour glu-
Sugar consumption: It is difficult to precisely deter- cose levels between 150 and 199 mg./ioo m l ) . In
mine levels of sugar intake in large populations. Table females, no significant change in cholesterol values was
3 gives the levels of dietary sugar in ten countries. We observed until two-hour glucose values reached 200
regard these figures as only rough estimates. Calcula- mg./ioo ml. This association between cholesterol and
tions based on data of the International Sugar Council26 glucose levels could reflect some direct relationship be-
suggest that sugar consumption in the United States is
roughly twice as high as in the Central American
TABLE 4
countries and many times higher than in Pakistan.
Relationship of age and plasma cholesterol in
Table 3 shows that there was a positive correlation be- Central America (2,034 subjects)
tween prevalence rate and sugar consumption (r =
.53). Although this association was not statistically Age Mean cholesterol (mg./lOO ml.)
Males Females
significant, the failure to demonstrate statistical signi- 35 to 44 142 141
ficance may be attributable to the relatively small num- 45 to 54 137 154
55 to 64 136 151
ber of populations (ten) for which data were avail- 65 to 74 139 149
able (see Discussion). 75 to 84 129 142
84* 119* 123*
Other dietary factors: There were also some rather
* Only ten males and eleven females were more than
consistent associations between prevalence of diabetes eighty-four years of age.

FEBRUARY, 1 9 7 1 103
INFLUENCE OF NUTRITIONAL FACTORS ON PREVALENCE OF DIABETES

TABLE 5
Relationship of plasma cholesterol to glucose tolerance in Central America*

Cholesterol (mg./lOOml.)
All subjects Males Females
Clearly normal tolerance 142 137 147
(2-hr, venous blood glucose <120mg./100 ml.)
High normal or borderline tolerance 142 139 145
(2-hr, value 120 to 149 mg./lOO ml.)
Slightly abnormal tolerance 152 166 140
(2-hr, value 150 to 199 mg./lOO ml.)
Grossly abnormal tolerance 173 179 168
(2-hr, value > 199 mg./lOO ml.)
* 2,034 subjects over thirty-four years of age.

tween these two factors; on the other hand, it may comparability of these different methods, so compari-
reflect only a relationship of both factors to some other sons among those countries where methods differed
factor or factors. Table 6 shows that there was some must be interpreted with this in mind. (The section
association between mean per cent of standard weight on Methods indicates which procedures were used in
and cholesterol level. The difference between the cho- each of the countries.) Mean levels of cholesterol were
lesterol levels of those above and below 109 per cent in East Pakistan, 133 m g . / i o o ml. (134 in males and
of standard weight is statistically significant. There 133 in females); in Malaya, 185 m g . / i o o ml. (182 in
was no difference in cholesterol levels of those with males and 188 in females); in Uruguay, 189 m g . / i o o
normal weight (90-109 per cent of standard weight) ml. (188 in males and 189 in females); and in Vene-
and those who were lean (less than 90 per cent of zuela, 211 m g . / i o o ml. (212 in males and 210 in
standard). The positive association between adiposity females). It is evident that there was a general asso-
and cholesterol values could mean that subjects with ciation between these levels of cholesterol and both
higher caloric intake (in relationship to energy expen- the prevalence of diabetes (table 3) and fatness
diture) tend to have both higher cholesterol levels and (figures 1 and 2 ) . There was also an association be-
lower glucose tolerance. tween cholesterol levels and several dietary factors, in-
cluding fat intake and animal fat consumption (table
There was a positive relationship in Central Amer- 3 ) . The correlation between prevalence of diabetes and
ica between "sociocultural" status9"14 and cholesterol mean cholesterol is significant statistically but it should
levels. In 271 males in whom sociocultural status was be kept in mind that the degree of association might
graded as "low," "medium" or "high," mean cholesterol have been greater or lesser if the same laboratory meth-
levels were 123, 138, and 147 m g . / i o o ml., respec- od had been used in all countries to measure choles-
tively. terol.
In Central America, there were no instances of Electrocardiographic findings: Table 7 shows the rela-
marked hypercholesterolemia among 2,034 subjects; the tionship between glucose tolerance and electrocardio-
highest value was 360 m g . / i o o ml. Six females graphic status in Central America. Although 1,645 indi-
(0.5 per cent) had values over 300 m g . / i o o m l , and viduals had both a glucose tolerance test and an electro-
only one male of the 803 tested had a plasma choles-
terol level exceeding 300 m g . / i o o ml. Very low
TABLE 6
cholesterol concentrations were common in both sexes.
Relationship of plasma cholesterol and adiposity
Values of less than 100 m g . / i o o ml. were observed in (per cent of standard weight) in Central America
18.8 per cent of males and 14.1 per cent of females. In
contrast to most other procedures which were standard- Weight as peri cent of Mean cholesterol (mg./lOOml.)
standard Male Females
ized, three different methods were used in the ten <80 138 146
countries in determining serum cholesterol levels. How- 80 to 89 127 142
90 to 99 142 140
ever, a common method was used in all Central Amer- 100 to 109 144 156
ican countries. W e have not adequately defined the >109 150 152

104 DIABETES, VOL. 2O, NO. 2


KELLY M. WEST, M.D., AND J O H N M. KALBFLEISCH, M.D.

cardiogram, the low prevalence of diabetes and the results will be published subsequently concerning these
infrequency of some electrocardiographic abnormalities electrocardiographic findings. We have considered the
made it impossible to determine their relationship to possibility that the higher rate of electrocardiographic
abnormal glucose tolerance. The prevalence of abnormal abnormality in those with impaired glucose tolerance
electrocardiograms was substantially greater in those might have been attributable to a greater electrocardio-
with abnormal glucose tolerance. Table 7 also shows graphic response to glucose loading in the hypergly-
the impressive relationship between abnormal glucose cemic subjects. We cannot exclude this possibility, but
tolerance and the prevalence of nonspecific T-wave it seems unlikely. Data were not systematically col-
changes. The number of older subjects was greater in lected concerning the temporal relationship between
the group with abnormal tolerance. This accounts to the load and electrocardiography, but the experimental
some extent for the higher rate of electrocardiographic conditions were the same for diabetics and nondia-
abnormalities in hyperglycemic subjects. But table 7 betics. It seems unlikely that the electrocardiographic
also indicates that the rate of electrocardiographic ab- changes which result from glucose loading are at-
normalities was much greater in those with hyper- tributable to hyperglycemia itself.26"27 We believe that
glycemia even when the data were age-adjusted. There the most likely explanation for the higher rate of elec-
was little difference between the sexes in the rate of trocardiographic abnormality in our diabetic subjects
electrocardiographic abnormalities. Tejada and his as- was an increased amount of coronary disease. Table 5
sociates had found previously that the difference be- shows that cholesterol levels were higher in the dia-
tween the sexes in coronary atherosclerosis was much
betics, and Robertson and Strong have recently demon-
less in Central America than in whites from New
strated that coronary atherosclerosis (gross pathology) is
Orleans.27
much greater in diabetics than nondiabetics in Costa
DISCUSSION Rica and Guatemala.28
The relatively high rate of electrocardiographic ab- Campbell and Cleve have assembled an impressive
normality (36 per cent in men and 39 per cent in array of evidence linking prevalence of diabetes and
women) was attributable to several factors including dietary sugar levels.6 Although the association between
the age distribution of the populations tested and the sugar consumption and prevalence of diabetes is not
glucose loading prior to electrocardiography. It should statistically significant in the ten countries to which our
also be kept in mind that the presence of any one of data apply, it would be statistically significant if this
many major or minor electrocardiographic changes such same degree of association were demonstrated in a
as left ventricular hypertrophy, ventricular extrasystoles, somewhat larger series. When our experience is added
bundle branch block, T-wave changes, etc., resulted in to that of Campbell and his associates,6 and when one
classifying the electrocardiogram as abnormal. Detailed considers the general association between sugar con-

TABLE 7
Rates of electrocardiographic abnormalities in Central America
and their relationship to glucose tolerance

Abnormal Nonspecific
ECG T-wave changes
Males Females Males Females
Subjects with clearly normal glucose 34% 37% 9% 14%
tolerance* (203 of 602) (312 of 837) (52 of 602) (114of 837)
Subjects with "borderline" glucose 60% 44% 20% 17%
tolerance* (18 of 30) (43 of 98) (6 of 30) (17 of 98)
85% 57% 39% 22%
Subjects with abnormal glucose tolerance* ( l l o f 13) (37 of 65) (5 to 13) (14of65)
36% 39% 10% 15%
All subjects (232 of 645) (392 of 1000) (63 of 695) (145 of 1000)
43% 43% 12% 16%
All subjects (age-adjusted)t
* This classification assumes that 2-hour glucose values more than 149 mg./lOO ml. are abnormal, those less than 120
mg./lOO ml. clearly normal, and those from 120 to 149 borderline,
t Adjusted to match age distribution of subjects with abnormal tolerance.

FEBRUARY, 197 I IO5


INFLUENCE OF NUTRITIONAL FACTORS ON PREVALENCE OF DIABETES

sumption and affluence, it seems highly probable that rural Uruguay is not due to a low prevalence of the
there is a significant association between sugar con- genetic trait or traits for diabetes, is suggested by the
sumption and the prevalence of diabetes. But the estab- fact that the relatives of these rural Uruguayans who
lishment of a statistically significant correlation would live in Montevideo have relatively high rates of dia-
not of course prove a cause and effect relationship. betes. Obesity is common in urban Uruguay.
Among our data are some impressive inconsistencies in Many other measurements were positively or nega-
this association. For instance, sugar consumption was tively associated with the prevalence of diabetes. Some
about the same in Malaya and Venezuela, but diabetes of these associations are clearly coincidental and have
was much more common in Venezuela (7.0 per cent) no direct cause and effect relationship. There was, for
than in Malaya (3.3 per cent). Diabetes was equally example, in the countries we studied, a good correlation
common in El Salvador and Malaya, but sugar con- between the gross national product per capita and the
sumption was much higher in Malaya. Some of the prevalence of diabetes. However, in examining these
data of Poon-King, Henry, and Rampersad29 are also data and the results of others, it is apparent that this
inconsistent with the hypothesis that the risk of dia- correlation is inconsistent after a level of income is
reached which permits a high caloric intake. For in-
betes increases in relation to sugar intake. Campbell and
stance, the Indians of Cherokee, North Carolina have
Cleave6 have suggested the imperfect relationship be-
incomes that are low by U.S. standards, but they con-
tween risk of diabetes and "sugar" intake may be at
sume more calories and have more diabetes than the
least in part the result of failing to take into account
rest of the nation.3 In New York City, certain poorer
the consumption of other refined carbohydrates (e.g.,
elements of the population are fatter than their more
in beer) which are often not identified as "sugar" in
affluent counterparts.30 But these "poor" New Yorkers
dietary surveys. They point out that refined carbohy-
and Cherokees are "rich" by standards of Asia or Cen-
drates may cause obesity because the satiety produced by tral America. Thus, the positive association between
these highly concentrated foods may be less than with diabetes and income which generally prevails over the
the more bulky "natural" foods. low spectrum of income levels is probably attributable
The negative association between the total amount of mainly to the effect of varying degrees of poverty on
carbohydrate consumed and the prevalence of diabetes the availability of calories.
is compatible with the hypothesis that the ingestion Our epidemiologic studies and those of others, which
of carbohydrate protects a population from developing indicate the very strong relationship between adiposity
diabetes. Yet certain findings argue against this. The and rate of diabetes, have been recently reviewed.1
well-fed subjects in Venezuela who consumed high The data in this paper extend and confirm our previous
levels of carbohydrate had a high prevalence of dia- observations in this regard. In contrast to the general
betes. The people of Central America have a relatively trend of this evidence, Jackson et al. found that a group
low rate of diabetes and high consumption of carbo- of fat African women had less diabetes than African
hydrates; but the small minority in Central America men and Indian women, both of whom were leaner.31
who are overweight also consume high levels of carbo- It was pointed out that the environment of the Afri-
hydrates, and they have a relatively high rate of dia- cans has been changing rapidly. Perhaps overnutrition
betes. Our data do clearly confirm that very high carbo- had not existed long enough to reflect the full risk of
hydrate diets are not necessarily associated with a pro- long term obesity. Also, the obese subjects of Jackson
pensity to diabetes. et al. had glucose loads which were slightly smaller in
There was also a general association between the rate relation to their extracellular spaces than the lean sub-
of diabetes and levels of dietary fat and protein. Hims- jects. The size of the load was constant irrespective of
worth proposed that diabetes might be caused by high the size of the subject. Nevertheless, the data of Jack-
levels of fat intake.7 Certain of our findings, however, son and his associates and other findings indicate that
appear to contradict this hypothesis. For instance, the environment and adiposity are by no means the sole
lean subjects we tested in the ranching country of rural determinants of prevalence. A study of glucose toler-
Uruguay have excellent glucose tolerance even though ance was made in a small population of Alaskan Eski-
they consume high levels of fat and protein. This sug- mos by Mouratoff, Caroll, and Scott.32 They found that
gests that neither protein nor fat in themselves pro- impairment of glucose tolerance was exceptionally rare
duce diabetes. That the low prevalence of diabetes in in Eskimos even though their weights in relation to

106 DIABETES, VOL. 2O, NO. 2


KELLY M. WEST, M.D., AND J O H N M. KALBFLEISCH, M.D.

heights exceeded those of a control population of nutrition, and diabetes in Uruguay, Venezuela, Malaya, and
whites. It was pointed out, however, that the Eskimos East Pakistan. Diabetes 15:9-18, 1966.
2
West, K. M., and Kalbfleisch, J. M.: Diabetes in Cen-
engaged in heavy physical exercise and were probably
tral America. Diabetes 19:656-63, 1970.
more muscular than the control group. Tulloch33 and 3
Stein, J. H., West, K. M., Robey, J. M., Tirador, D. R,
Pyke34 have recently published good review articles con- and McDonald, G. W . : The high prevalence of abnormal
cerning the epidemiology of diabetes. glucose tolerance in the Cherokee Indians of North Caro-
Our studies reported here and elsewhere1'3 included lina. Arch. Intern. Med. 116:842-45, 1965.
4
many races (Hindu and Moslem Indians, North Amer- O'Sullivan, J. B., Cosgrove, J., and McCaughan, D.:
Blood sugars, vascular abnormalities and survival: The Ox-
ican Indians, Central American Indians, Malays, Chi-
ford study after 17 years. Postgraduate Med. J. 955-59, 1968.
nese, and "whites" from widely differing ethnic 5
Vallance-Owen, J.: Causation of diabetes. Proceedings of
groups). Among these races, the prevalence of dia- the Royal Society of Medicine 55:207-10, 1962.
betes varied substantially but these differences were 6
Cleave, T. L., and Campbell, G. D . : Diabetes, coronary
small when races were matched for fatness.1'- To thrombosis and the saccharine disease. Bristol, John Wright
the extent that dietary sugar adds to, rather than re- & Sons, Ltd., 1969.
7
Himsworth, H. P.: Diet and the incidence of diabetes
places, other sources of calories, it would increase adi-
mellitus. Clin. Sci. 2:117-48, 1935-6.
posity. Our data do not exclude the possibility that 8
Interdepartmental Committee on Nutrition for National
high levels of sugar consumption increase susceptibility Defense: Manual for Nutrition surveys, 2nd Ed., Washing-
to diabetes by a mechanism independent of their effect ton, D.C., 1963.
9
on caloric intake. Although the epidemiologic evidence Publication V-25 of the Institute of Nutrition of Cen-
is by no means conclusive in this regard, we believe tral America and Panama. Evaluacion Nutricional de la Po-
blacion de Centre America y Panama: Guatemala. Guate-
that fatness (irrespective of its cause) is probably
mala City, 1969.
more deleterious than high levels of dietary sugar. 10
Publication V-26 of the Institute of Nutrition of Cen-
Certain recent observations from the laboratory support tral America and Panama. Evaluacion Nutricional de la Pobla-
this view. For example, it is now evident that adiposity cion de Centro America y Panama: El Salvador, Guatemala
causes hyperinsulinism35'36 which declines with weight City, 1969.
11
reduction.37-38 Another pertinent recent finding is that Publication V-28 of the Institute of Nutrition of Central
America and Panama. Evaluacion Nutricional de la Poblacion
certain protein-carbohydrate mixtures produce a much de Centro America y Panama: Costa Rica. Guatemala City,
greater beta cell response than carbohydrate alone.39 1969.
Finally, we note the very low rates of diabetes in Asian 12
Publication V-27 of the Institute of Nutrition of Central
populations where carbohydrate (mainly rice) con- tral America and Panama. Evaluacion Nutricional de la
sumption is quite high. Poblacion de Centro America y Panama. Nicaragua. Guate-
mala City, 1969.
13
ACKNOWLEDGMENT Publication V-29 of the Institute of Nutrition of Central
tral America and Panama. Evaluacion Nutricional de la Po-
A detailed list of participants in the studies in Cen- blacion de Centro America y Panama. Honduras. Guatemala
tral America is part of the publications relating to the City, 1969.
specific countries.9"14 Lists of the principal participants 14
Publication V-30 of the Institute of Nutrition of Cen-
in the diabetes-related studies have been published tral America and Panama. Evaluacion Nutricional de la Po-
blacion de Centro America y Panama: Panama. Guatemala
elsewhere.1'2 The nutrition surveys in Central America
City, 1969.
were sponsored by the Institute of Nutrition of Cen- 15
Grace, C. S., and Goldrick, R. B.: Assessment of body
tral America and Panama, the Nutrition Program of composition in normal and obese subjects. Aus. Ann. Med.
the U.S. Public Health Service (formerly Office of 28:26-31, February 1969.
16
International Research), and the governments of the Z a k , B., Dickerson, R. C , White, E. F.: Burnett, H., and
six republics. We are especially indebted to Edwin Chervey, P. J.: Rapid estimation of free and total cholesterol.
Amer. J. Clin. Path. 24:1307-15, 1954.
Bridgforth, M.S., William McGanity, M.D., Guillermo 17
Searcy, R. L., Bergquist, L. M., and Jung, R. C.: Rapid
Arroyave, Ph.D., Werner Ascoli, M.D., and Arnold ultramicro estimation of serum total cholesterol. J. Lipid Res.
Schaefer, Ph.D., for advice and assistance in planning 1:349-51, i960.
18
and conducting those aspects of the nutrition studies Carpenter, K. J., Gotsis, A., and Hegsted, D. M.: Esti-
relating to diabetes. mation of total cholesterol in serum by a micro method. Clin.
Chem. 3:233-38, 1957.
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West, K. M., and Kalbfleisch, J. M.: Glucose tolerance, changes induced by the taking of food. Amer. Heart J. 17:

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725-27, 1939. Baltimore, T h e W i l l i a m s and W i l k i n s Company, p p . 538-51,


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Simonson, E., Alexander, H., Henschel, A., and Keys, 1968.
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A . : T h e effects of meals on the electrocardiogram in normal Poon-King, T., Henry, M. V., and Rampersad, F.: Pre-
subjects. Amer. H e a r t J. 3 2 : 2 0 2 - 1 4 , 1946. valence and natural history of diabetes in Trinidad. Lancet
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Sears, G. A., and M a n n i n g , G. W . : Routine electrocardi-
1:155-60, 1968.
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ography: postprandial T-wave changes. Amer. H e a r t J. j d : G o l d b l a t t , P. B., Moore, M. E., and Stunkard, A. J.:
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R o c h l i n , I., and Edwards, W . L. J . : T h e misinterpreta- Jackson, W . P. U., Goldberg, M. D., Marine, N . , and
iton of electrocardiograms with postprandial T-wave inver- Vinik, A. L.: Effectiveness, reproducibility and weight-rela-
sion. Circulation 1 0 : 8 4 3 - 4 9 , 1954. tion of screening tests for diabetes. Lancet 2 : 1 1 0 1 - 0 5 , 1968.
32
23
Ostrander, L. D . , Jr., and Weinstein, B. J . : Electro- Mouratoff, G. J., Carroll, N . V., and Scott, E. M . : Dia-
cardiographic changes after glucose ingestion. Circulation 30: betes mellitus in Eskimos. J A M A 199:961-66, 1967.
33
67-76, 1964. Tulloch, J. A . : Diabetes in Africa: In Diabetes Mellitus,
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Dear, H . D . , Bruncher, C. R., and Sawayama, T . : L. J. P. Duncan, Ed. E d i n b u r g h University Press, 1966, p . 115.
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Changes in electrocardiogram and serum potassium values fol- Pyke, D . A.: Geography of diabetes. Postgrad. Med. J. 45
lowing glucose ingestion. Arch. Intern. Med. 1 2 4 : 2 5 - 2 8 , (supplement on diabetes) : 7 9 6 - 8 0 1 , 1969.
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1969. K a r a m , J. H., Grodsky, G. M., Forsham, P. H . : Excessive
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Height, and Selected Body Dimensions of Adults, United immunochemical assay. Diabetes 12:197-204, 1963.
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States, 1960-62. U.S. D e p a r t m e n t of Health, Education and Bierman, E. L., Bagdade, J. D., and Porte, D . : Obesity
Welfare, W a s h i n g t o n , D.C., 1965. and diabetes: T h e odd couple. Amer. J. Clin. N u t r . 2 1 : 1 4 3 4 -
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Sugar Year Book, London, International Sugar Council,
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1963. F a r r a n t , P. C , Neville, R. W . , Stewart, G. A.: Insulin
27 release in response to oral glucose in obesity: T h e effect of
Tejada, C , Strong, J. P., Montenegro, R., Restrepo, C ,
and Solberg, L.: Distribution of coronary and aortic athero- reduction of body weight. Diabetologia 5:198-200, 1969.
38
sclerosis by geographic location, race and sex. In T h e Geo- Albrink, M. J.: Overnutrition and the fat cell. In D u n -
graphic Pathology of Atherosclerosis, H . C. McGill, Jr., Ed. can's Diseases of Metabolism. 6th Ed., P. K. Bondy, Ed.
Baltimore, T h e W i l l i a m s and W i l k i n s Company, 1 8 : 5 0 9 - Philadelphia, W . B. Saunders, 1969, p . 1267.
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26, 1968. Floyd, J. C , Jr., Fajans, S. S., Pek, S., Thiffault, C A.,
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Robertson, W . B., and Strong, J. P . : Atherosclerosis in Knopf, R. F., and Conn, J. W . : Synergistic effect of essential
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TOX DIABETES, VOL. 2O, NO. 2

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